Bibliography on Refinement and Environmental Enrichment for Primates. Enrichment 5-9

(5) Promoting Arboreal Behavior

(5,1) The Importance of Access to Vertical Dimension of Space

Bernstein IS, Draper WA 1964. The behaviour of juvenile rhesus monkeys in groups. Animal Behaviour 12, 84-91
Subjects spent 48%-72% of the time in the upper one-third of the compound.

Bloomsmith MA, Lambeth SP, Haberstroh MD 1999. Chimpanzee use of enclosures. American Journal of Primatology 49, 36
Group-housed chimpanzees spent 43% of their time off the ground.

Buchanan-Smith HM 1991. A field study on the red-bellied tamarin, Saguinus l. labiatus, in Boliva. International Journal of Primatology 12, 259-276
Tamarins spent 90% of their time in the upper half of their 186 cm-high cages when observations were made from a hide.

Clarence WM, Scott JP, Dorris MC, Paré M 2006. Use of enclosures with functional vertical space by captive Rhesus monkeys (Macaca mulatta) involved in biomedical research. JAALAS [Contemporary Topics in Laboratory Animal Science] 45(5), 31-34
"The monkeys visited more often and occupied for longer time regions at or above human eye level [perches and top home cage] than lower regions." The total percentage of time spent in the top home cage was found to be significantly greater than in the bottom home cage."

European Commission 2002. The Welfare of Non-human Primates - Report of the Scientific Committe on Animal Health and Animal Welfare. European Commission, Strasbourg, France
http://europa.eu.int/comm/food/fs/sc/scah/out83_en.pdf
"Enclosures for nonhuman primates should be equipped with one or more elevated resting surfaces (to a postion higher than the level at which they perceive threatening factors, e.g., humans) and installed in such a way that an animal can sit on them comfortably. Perches or shelves should be provided in all cages. Arboreal species should be given adequate vertcial space to allow the expression of normal locomotry behaviour. Primates should not be placed in double-tiered caging unless the arrangement permits adequate vertical movement for the animal."

Goff C, Howell SM, Fritz J, Nankivell B 1994. Space use and proximity of captive chimpanzees (Pan troglodytes) mother/offspring pairs. Zoo Biology 13, 61-68
"Results confirmed the importance of vertical cage dimension and suggested the provision of horizontal substrates above the enclosure floor is important."

Home Office 1989. Animals (Scientific Procedures) Act 1986. Code of Practice for the Housing and Care of Animals Used in Scientific Procedures. Her Majesty's Stationery Office, London
"The use of space by primates means that cage volume is important. Virtually all show a vertical flight reaction. Cage height should allow for this and should permit the animals to stand erect, jump and climb, and to sit on a perch without head or tail touching the cage."

International Primatological Society 1993. IPS International guidelines for the acquisition, care and breeding of nonhuman primates, Codes of Practice 1-3. Primate Report 35, 3-29
"The vertical dimension of the cage is of importance [because of the vertical flight response] and cages where the monkey is able to perch above human eye level are recommended."

Kaumanns W, Schönmann U 1997. Requirements for cebids. Primate Report 49, 71-91
"Arboreal species need cages and enclosures which allow a differentiated moving in the vertical dimension. They should be able to use spatial positions which are above the level of the position of certain groupmates and of threatening humans or potential dangerous events in their environment. Cage positions in a keeping room below the eye level of human can be a source of permanent stress, because they are incompatible with adaptive tendencies of arboreal primates to avoid risks by using higher parts of the habitat."

MacLean E, Roberts Prior S 2006. View from the top. AWI (Animal Welfare Institute) Quarterly 55(3), 7
"Across both conditions, monkeys showed a strong preference for the upper-row cage indicating that elevation was more important than illumination in guiding location preference. Although monkeys did increase the amount of time that they spent in the lower row during periods of reversed lighting, this trend was not significant. Nonetheless, we do not interpret this result as evidence that sufficient lighting is not important to captive monkeys. Rather, we believe that monkeys' consistent preference for the upper-row reflects the paramount importance of access to elevated space."

National Research Council 1998. The Psychological Well-Being of Nonhuman Primates. National Academy Press, Washington
"Under natural conditions, many primates spend much of their lives aboveground and escape upward to avoid terrestrial threats. Therefore, these animals might perceive the presence of humans above them as particularly threatening. ... Even macaques, which some describe as semiterrestrial, spend most of the day in elevated locations and seek the refuge of trees at night. ... Optimal use of available cage space might well depend more on the placement of perches, platforms, moving and stationary supports, and refuges than on cage size itself."

Reinhardt V, Liss C, Stevens C 1996. Space requirement stipulations for caged nonhuman primates in the United States: A critical review. Animal Welfare 5, 361-372
"Having no stimulatory value, space alone does not enhance an animal's environment. ... Legal space requirements for non-human primates are not adequate unless they stipulate that sufficient height be provided to accommodate properly placed elevated structures."

Ross SR, Lukasb KE 2006. Use of space in a non-naturalistic environment by chimpanzees (Pan troglodytes) and lowland gorillas (Gorilla gorilla gorilla) . Applied Animal Behaviour Science 96, 143-152
"Chimpanzees preferred the highest tier of the enclosure and the gorillas preferred the floor level. Both species showed preferences for doorways, corners and the mesh barriers adjacent to keeper areas."

Taylor L, Owens A 2004. Enclosure use by aged squirrel monkeys (Saimiri sciureus). American Journal of Primatology 62(Supplement), 85
A group of squirrel monkeys was translocated from an indoor exhibit to an outdoor enclosure. "The monkeys were scored most often among the largest and highest branches in the tallest tree in the enclosure (17.7% ). .. None were ever scored on the ground, despite the water source being there and the insect foraging opportunities.”

Tecot S, Jensvold ML, Fouts R 1999. Evaluation of an enriched physical environment: space and structure utilization in Pan troglodytes. American Journal of Physical Anthroplogy Supplement 264, 264
Ethological findings indicate that "access to vertical structures is important to these [group of five] chimpanzees."

Westlund K Preference of the vertical dimension of cyno pairs living in high cages. Laboratory Animal Refinement and Enrichment Forum (electronic discussion group), November 28, 2002
"In a quantitative study I did on pair-housed cynos the animals spent 95% of their waking time in the upper part of the cage (being housed in a system that resembles a double-tier system, but with vertical access to upper and lower sections) - which suggests that their preference along the gradient of height is unequivocal! No bedding was provided on any of the cage floors, and all food was given in the bottom section. Even so, animals would bring the food to the upper part and consume it there."

(5,2) Elevated Structures

Abee CR 1985. Medical care and management of the squirrel monkey. In Handbook of Squirrel Monkey Research Rosenblum LA, Coe CL (ed), 447-488. Plenum Press, New York
"Squirrel monkeys .... lack ischeal callosities and therefore are prone to the development of sores if they are not provided with suitable structures on which to climb and perch. Squirrel monkeys prefer a flat, shelf-type surface for sleeping, but animals using such perches frequently develop pressure ulcers on the dorsal aspect of the tail. By using large-diameter plastic pipe (1.5 inch), a highly desirable perch can be provided. These perches have a broad surface yet are sufficiently contoured to avoid tail sores."

*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 4.17. Vertical Space Enhancement. Washington, DC: Animal Welfare Institute
"Most of the primates' natural environment is "fixed." Even a tree is "fixed;" it's only at the end of branches where a monkey in nature would have the sensation of anything like a swinging perch. A fixed perch is a great thing for a monkey. We used to hang numerous swings and movable raised structures into the enclosure of our group-housed cynos, but we could see very clearly that they prefer the stable perches or platforms. Our animals very rarely used ropes or swings. The only ones using those elements were babies and juveniles.
In the caging systems we use there is no bottom tier. All cages are 0.6 m off of the floor. Each cage is furnished with a 1 m high perch; so it is pretty much at human eye level 1.6 m height. It seems to me that the animals feel relaxed when they sit on their perch and can meet me at eye level. A low perch has little or no value as a "safe" resting location from our monkeys point of view."

Bayne K, Hurst JK, Dexter SL 1992. Evaluation of the preference to and behavioral effects of an enriched environment on male rhesus monkeys. Laboratory Animal Science 42, 38-45
"With simultaneous exposure, the single-housed subjects spent the greatest portion of the interactive time [30 minute-observation sessions] on the perch [16.8%], the second greatest amount of time spent divided approximately equally between interacting with the Kong [5.0%] and Tug-A-Toy [4.9%], and the least amount of time spent manipulating the grooming board [0.4%]."

Brinkman C 1998. Usefulness of swings for macaques . Primate Enrichment Forum (electronic discussion group), (August 17, 1998)
"I have used swings with cynos (socially and singly housed) and pigtails (socially housed). My impression is that adult animals do not really use them, that is, to 'swing'. Young animals like moving things, be they swings, or other suspended items. My adults did not even use the swings much to perch on; my explanation is that on a swing, you simply cannot easily relax. Animals cannot really sit on them, and especially with the cynos, you can see almost continuous movement in the tail, compensating in balance."

Crockett CM, Bellanca RU, Bowers CL, Bowden DM 1997. Grooming-contact bars provide social contact for individually caged laboratory primates. Contemporary Topics in Laboratory Animal Science 36(6), 53-60
"Monkeys in upper cages averaged 48%±27% SD of the time on the perch, compared with 40%±25% SD for monkeys in lower cages."

Davis E 2006. More fun with a barrel full of monkeys: A nonhuman primate swing made by recycling plastic barrels. Laboratory Primate Newsletter 45(3), 9-11
"The NIH Shared Animal Facilities' enrichment program has developed a primate swing created from recycling our discarded plastic 30- and 55-gallon detergent barrels. These swings are easy to construct and are effective in increasing our animals' behavioral repertoires. Additionally, these swings are safe, portable, non-toxic, easy to sanitize, and almost indestructible. We have used these barrels in our socially-housed monkey runs for over three years, and they are still going strong!"

Dexter SL, Bayne K 1994. Results of providing swings to individually housed rhesus monkeys (Macaca mulatta). Laboratory Primate Newsletter 33(2), 9-12
The single-housed adult test subjects manipulated the swings but showed little inclination to actually use them for swinging.

European Commission 2002. The Welfare of Non-human Primates - Report of the Scientific Committe on Animal Health and Animal Welfare. European Commission, Strasbourg, France
Comprehensive updated recommendations on the species-appropriate care of nonhuman primates.
"Enclosures for nonhuman primates should be equipped with one or more elevated resting surfaces (to a postion higher than the level at which they perceive threatenign factors, e.g., humans) and installed in such a way that an animal can sit on them comfortably. Perches or shelves should be provided in all cages."

Günther MM 1998. Influence of habitat structure on jumping behaviour in Galago moholi. Folia Primatologica 69 (Supplement 1), 410
There was a statistically significant preference for wooden perches versus PVC perches and for high perches versus low perches. "These results suggest that support material [perches], as well as height, influences the behaviour of G. maholi and these should be taken into consideration in behavioural and biomedical studies as well as in the construction of cage facilities. Studies which do not take these factors into account are to some extent vitiated."

Howell SM, Mittra E, Fritz J, Baron J 1997. The provision of cage furnishings as environmental enrichment at the Primate Foundation of Arizona. The Newsletter 9(2), 1-5
"Adults infrequently used 'moving' furnishings (e.g., swinging ropes, hanging tubes, etc...) and seemed to prefer 'stable' horizontal furnishings (e.g., benches, logs) above the enclosure floor."

Kopecky J, Reinhardt V 1991. Comparing the effectiveness of PVC swings versus PVC perches as environmental enrichment objects for caged female rhesus macaques. Laboratory Primate Newsletter 30(2), 5-6
Single-housed subjects' "preference for perches was probably related to the fact that perches, unlike swings, are fixed structures permitting continuous relaxed postures rather than short-term balancing. Moreover, perches, unlike swings, permit the animals to sit right in front of the cage with optimal visual control of the environment outside of the cage."

Millere KE, Laszlo K, Suomi SJ 2006. Using recycled barrel swings vs. Prima-Hedrons in primate enclosures. Laboratory Primate Newsletter 45(3), 12
"To document the utility of using recycled barrel swings vs. Prima-Hedronsâ as enrichment objects, we observed a socially housed group of 28 tufted capuchins (Cebus apella). .. We found no significant difference in the average frequency of use of hanging Prima-Hedrons vs. hanging barrels."

Neveu H, Deputte BL 1996. Influence of availability of perches on the behavioral well-being of captive, group-living mangabeys. American Journal of Primatology 38, 175-185
"A total deprivation of perches yielded an increase in aggressive behaviors and locomotion, and a decrease in cohesiveness. Placing perches progressively in the experimental cage restored the level of all the variables to levels found in the control cage [with five perches]. ... Therefore, perches constitute a necessary feature of an adequate environment for mangabeys."

O'Neill-Wagner PL 1994. When trying to get your monkeys to behave, try perches. In Touch 1(2), 6-8
The group-housed animals preferred perches at high elevation over perches at low elevation.

Ochiai T, Matsuzawa T 1999. Environmental enrichment for captive chimpanzees (Pan troglodytes): Introduction of climbing frames 15 m high [Japanese text with English summary]. Reichorui Kenkyu/Primate Research 15, 289-296
"Tall climbing frames were introduced into an outdoor compound for captive chimpanzees as a way of environmental enrichment. ... Chimpanzees spent 81% of the observation time on the climbing structures. ... All chimpanzees used the climbing structure throughout the day with little individual difference."

Phillippi-Falkenstein K 1998. Usefulness of swings for macaques. Primate Enrichment Forum (August 19, 1998)
"In group runs, corncribs and corrals, swings provide a dimension of environmental complexity for rhesus and pig-tailed macaques. The swings are primarily used by young animals, while adults rarely use them. Tire swings seem to be the favorite. It has been my experience that the animals - even juveniles - do not benefit from swings when housed in 'small' standard cages: They simply don't use them."

Plesker R, Herzog A 2001. Prima hedrons, puzzle feeders and television as environmental enrichment for captive African Green Monkeys. Primate Eye , 4
"The prima hedrons had no significant effect on any of the behaviours investigated. These were infrequently used as objects for playing, resting or observation."

Reinhardt V 1989. Evaluation of the long-term effectiveness of two environmental enrichment objects for singly caged rhesus macaques. Lab Animal 18(6), 31-33
"The singly caged monkeys spent on average 28% of the total observation time [120 min] with the PVC pipes. ...While perching, the monkeys sat in front of the cage for 95% of the time, in the middle or rear of the cage for 5% of the time. ... The proportion of time spent with the pipes was three times greater for animals living in lower-row cages than for animals living in upper-row cages. ... In the elevated position, the light exposure was increased, a fact that made the pipes of particular value for the lower-row cages animals."

Reinhardt V, Pape R 1991. An alternative method for primate perch installation. Lab Animal 20(8), 47-48
Modification of squeeze cages is described allowing the installation of a perch that does not interfere with the normal operation of the cage.

Reinhardt V 1990. Comparing the effectiveness of PVC perches versus wooden perches as environmental enrichment objects for singly caged rhesus monkeys. Laboratory Primate Newsletter 29(1), 13-14
"One half of each cage was provided with a PVC pipe, the other with an oak branch." Both perches had the same diameter and were installed in the same manner. During one-hour observation sessions, single-caged subjects showed no clear preference but spent on average 19% of the time on the PVC pipe and another 24% of the time on the oak branch.

Reinhardt V 1992. Environmental enrichment branches that do not clog drains. Laboratory Primate Newsletter 31(2), 8
"More than 700 caged rhesus and stump-tailed macaques housed in 29 rooms have been exposed to red oak perches and/or loose branch segments for a period of six months. Drains did not clog in any of the 29 rooms during this time although the animals gnawed the wood extensively."

Reinhardt V 1992. Space utilization by captive rhesus macaques. Animal Technology 43, 11-17
"The area covered by the floor was 3 times larger than that covered by elevated structures; nonetheless the animals were located significantly more often (89.8% of 108 scan samples) on elevated structures than on the floor (8.6% of 108 scan samples). ... The higher an animal's rank position, the more pronounced was its habit to utilize high-level (>130 cm above floor) structures of the pen, while low ranking animals had to be content with low-level structures (40 cm above floor) and the floor. ..
All members of the group would inevitably take to elevated sites whenever they heard or saw fear-inducing personnel. ... The animals huddled together with regularity on high-level structures but never on low-level structures or on the floor. ... It was concluded that [group-housed] laboratory rhesus macaques prefer the vertical dimension over the horizontal dimension as primary living space."

Reinhardt V 2003. Legal loophole for subminimal floor area for caged macaques. Journal of Applied Animal Welfare Science 6, 53-56
"The USDA regulations pertaining to the minimum space requirements of nonhuman primates and the fitting of elevated resting surfaces are contradictory. They implicitly condone the prevailing perch design that allows maximal usage of animal room space by stacking the cages on top of each other but fails to address the animals minimal spatial needs for normal postural adjustments with freedom of movement. An amendment to the regulations is needed to clarify that perches, ledges, swings, or other suspended fixtures have to be installed in such a way that they do not block part of the minimum floor space that is needed by an animal to make species-typical postural adjustments with freedom of movement."

Ricker RB, Williams LE, Brady AG, Gibson SV, Abee CR 1995. Environmental enhancement for laboratory-housed squirrel monkeys: Fifteen-year retrospective analysis of procedures. Contemporary Topics in Laboratory Animal Science 34(4), 55
"Two types of perching material were tried: polyvinyl chloride (PVC) and hemp (rope). The PVC was preferred by the animals and was set up in multiple levels, allowing use of vertical as well as horizontal space."

Schmidt EM, Dold GM, McIntosh JS 1989. A perch for primate squeeze cages. Laboratory Animal Science 39, 166-167
Modification of single squeeze-cages is described allowing the installation of a perch that does not interfere with the normal operation of the cage. "The monkeys make use of their perch for feeding, grooming and sleeping" for 30% to 95% of the day.

Seier JV 2000. Usefulness of wooden material for environmental enrichment for rhesus macaques. Primate Enrichment Forum (February 12, 2000)
"We have been using wood extensively in our vervet monkey colony (about 300 monkeys, indoors) and communal cages we make climbing apparatus from wood. Wood perches for resting were also installed but they use the metal perches equally well. ...The vervets use the wood as described for other species, stripping the bark and climbing. They eventually reduce and medium branches to a single pole. We find this desirable since it keeps them occupied for hours. ... They do not loose interest in the wood as they do in other objects which we have tried. ... There is obviously the problem of sanitation but we replace the wood regularly and autoclave it before we place inside the cage (luckily we have a very large autoclave). Clogging of drains and mould has not occurred, neither have problems such as injury through splintering. ... We consider wood as our most important enrichment tool."

Shimoji M, Bowers CL, Crockett CM 1993. Initial response to introduction of a PVC perch by singly caged Macaca fascicularis. Laboratory Primate Newsletter 32(4), 8-11
"Longtailed macaques ... exhibit a vertical flight response when alarmed. Therefore, the height of the cage is important for allowing the animals to withdraw from potentially stressful or alarming situations. ..Single-housed "monkeys spent significantly more time clinging to the cage wall ("suspended") in the absence of the perch. ... Monkeys in lower level cages [26% of daytime] averaged somewhat more time on the perch than those in upper cages [14% of daytime]. ... There was less stereotypy when the perch was present."

Smith K, St. Claire M, Byrum R, Harbaugh S, Harbaugh J, Erwin J 2003. Use of space, cage features, and manipulable objects by laboratory primates: individual differences and species variability. American Journal of Primatology 60(Supplement), 76-77
http://www.asp.org/asp2003/abstractDisplay.cfm?abstractID=625&confEventID=514
”Rhesus (74%), longtailed (71%), vervets (94%), and patas (82%) significantly exceeded the expected rate of perch use (25%), while pigtailed (28%) did not differ from expectation.”

Taylor LL 1998. Promoting species typical behavior in Coquerel's sifakas (Propithecus Verreauxi Coquereli). American Zoo and Aquarium Association (AZA) Regional Conference Proceedings, 599-603
"The sifakas rarely were observed on the ground, preferring to locomote on vertical substrates and rest on vertical and horizontal elevated substrates in all four size categories. Therefore, if vertical surfaces were absent from captive habitats, these rare lemurs could not display their preferred mode of arboreal locomotion. Further, the rarity of ground use highlights the need for elevated feeding sites."

Taylor L, Owens A 2004. Enclosure use by aged squirrel monkeys (Saimiri sciureus). American Journal of Primatology 62(Supplement), 85
A group of squirrel monkeys was translocated from an indoor exhibit to an outdoor enclosure. “Static substrates were preferred (64.3%). Dynamic substrates, like rope walkways, were used primarily during locomotion (33.8%) from one static location to another.”

van Wagenen G 1950. The monkeys. In The Care and Breeding of Laboratory Animals Farris EJ (ed), 1-42. John Wiley, New York
"Sitting on the board [approximately 1 m off the ground of the room], facing the center of the room, is the favorite position of the monkeys. At this height these intensely alert animals have a better view of activities within the room, and they can meet visitors on the same eye level. ... and they sleep on the board at night."

Watson DSB 1991. A built-in perch for primate squeeze cages. Laboratory Animal Science 41, 378-379
Perch installation design for single squeeze-back cages is described. "Independent of gender the monkeys were seen using their perches more than 84% of the time."

Watson SL, Shively CA 1996. Effects of cage configuration on behavior in cynomolgus macaques. XVIth Congress of the International Primatological Society/XIXth Conference of the American Society of Primatologists, Abstract No. 674
"Stereotypies occurred more often in the STD [standard single cage] than in the VE [vertically-enhanced; probably with perche(s)]. ... The results indicate that VE cages provide more suitable individual housing environments for nonhuman primates than STD cages."

Watson SL, Gray A, Taylor E, Johnson B, Fahm B, McGee A, Bingham W, Banks P 2002. Efficacy of environmental enrichment for garnett's bushbaby (Otolemur garnettii). American Journal of Primatology 57, 38-39)
"Bushbabies interacted with swinging/climbing apparati significantly more than with manipulanda.... All animals spent significantly more time at the top than at the bottom of their cages (t(17)=3.3, p=.004). ... These results suggest that provision of vertical space and swinging/climbing opportunities may be more effective forms of enrichment for bushbabies than provision of manipulanda."

Williams LE, Abee CR, Barnes SR, Ricker RB 1988. Cage design and configuration for an arboreal species of primate. Laboratory Animal Science 38, 289-291
"Squirrel monkeys preferred a poly-vinyl-chloride pipe perch (rigid) over rope perches (non-rigid). For an arboreal animal, a higher perch may be perceived as safer." Additional perches decreased the propensity for development of tail ulcers associated with floor contact. "With only one perch level, males were forced to spend a large percentage of their time sitting on the floor rather than the main perches [which were occupied by females]."

Wolff A 1989. Polyvinyl chloride piping as perch material for squirrel monkeys. Laboratory Primate Newsletter 28(1), 7
"An additional unexpected benefit of the PVC piping has been a decrease in dorsal tail-head abrasions, frequently seen in squirrel monkeys that sit on the stainless steel flooring of standard primate cages."

Woodbeck T, Reinhardt V 1991. Perch use by Macaca mulatta in relation to cage location. Laboratory Primate Newsletter 30(4), 11-12
Single-housed "animals living in lower-row cages spent an average of 31.6% of the time perching on their pipes while animals living in upper-row cages perched only 6.9% of the time. Access to the vertical dimension of the cage was more important for the lower-row caged monkeys who continuously live close to the ground, in the horizontal dimension of the room."

(6) Promoting Object-oriented Behavior

(6,1) Commercial Toys

Anonymous 1991. The psychological well-being of primates. Primate News 25(Fall), 3-5
"The problems with all these devices is that they are expensive to purchase (foraging boards cost $60 each) and to maintain (they require many hours to fill and clean). "That is tough on an institution like ours," says Dr. Kelley, "that has a large colony of animals. We could live with the expense if we were certain that these devices really improve the well-being of the animals. It seems, however, that after a short time the animals lose interest in foraging boards, and fleece boards, just as they lose interest in balls and toys."

Bayne K 1989. Nylon balls re-visited. Laboratory Primate Newsletter 28(1), 5-6
"Approximately 10% of the [single-housed] monkeys in a room utilize the ball [Nylaball®]at any given time."

Bayne K, Hurst JK, Dexter SL 1992. Evaluation of the preference to and behavioral effects of an enriched environment on male rhesus monkeys. Laboratory Animal Science 42, 38-45
"With simultaneous exposure, the single-housed subjects spent the greatest portion of the interactive time [30 minute-observation sessions] on the perch [16.8%], the second greatest amount of time spent divided approximately equally between interacting with the Kong [5.0%] and Tug-A-Toy [4.9%], and the least amount of time spent manipulating the grooming board [0.4%]."

Bayne K, Dexter SL, Hurst JK, Strange GM, Hill EE 1993. Kong toys for laboratory primates: Are they really an enrichment or just fomites? Laboratory Animal Science 43, 78-85
"The use of simple toys for environmental enrichment of laboratory primates is an economical means of increasing the complexity of the cage environment to a limited degree. The limitations presented by this method of enrichment include the finite ways in which a simple device can elicit normative behaviors and the relatively rapid habituation to the device." It was demonstrated that microbial growth can persist on enrichment devices - such as Kong toys - after they have been sanitized in a commercial cagewasher.

Bloomsmith MA, Finlay TW, Merhalski JJ, Maple TL 1990. Rigid plastic balls as enrichment devices for captive chimpanzees. Laboratory Animal Science 40(3), 319-322
"The mean percentage of ball-use time for all subjects during the study [first ten hours after initial presentation] was 7.1%. ... Age and housing effects were obtained, with younger animals and those housed in more barren environments exhibiting higher levels of ball use. It is concluded that the balls were worthwhile additions to the chimpanzee environments with use stabilizing at a mean of 2.5% of the subjects' time."

Brent L, Stone AM 1998. Destructible toys as enrichment for captive chimpanzees. Journal of Applied Animal Welfare Science 1, 5-14
Nine singly caged chimpanzees were provided with eight different toys made of plastic, vinyl, or cloth one at a time or several at once. The toys remained in the cages an average of three days. "The chimpanzees varied greatly in their interest in the toys. One subject rarely contacted the toys and others used them a great deal and quickly destroyed them."

Cardinal BR, Kent SJ 1998. Behavioral effects of simple manipulable environmental enrichment on pair-housed juvenile macaques (Macaca nemestrina). Laboratory Primate Newsletter 37(1), 1-3
"The teddy bear was preferred as a manipulable toy over the pink teething ring and the green teething ring. Toy use declined with time, indicating that rotation of toys, at least in the short term, may increase use."

Crockett CM, Bielitzki JT, Carey A, Velez A 1989. Kong toys as enrichment devices for singly-caged macaques. Laboratory Primate Newsletter 28(2), 21-22
"Providing objects such as Kong toys to macaques in single-animal housing with little or no opportunity for manipulation is mildly enriching to some of the monkeys. Periodically removing and reintroducing the toys would increase their enrichment value."

Hamilton P 1991. Enrichment toys and tools in recent trials. Humane Innovations and Alternatives in Animal Experimentation 5, 272-277
"When toys were left with an animal for several days, the individual became accustomed to and desinterested in the toy."

Kessel AL, Brent L 1998. Cage toys reduce abnormal behavior in individually housed pigtail macaques. Journal of Applied Animal Welfare Science 1, 227-234
"Providing multiple manipulable toys as enrichment for [single-caged] pigtail macaques was effective in reducing abnormal behavior" during 30-min observation session. "The use of the toys was reduced over time."

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
"Our experience with cage toys suggests that after a very short time (a few days or less), most macaques will lose interest in the objects that are offered."

Novak MA, Musant A, Munroe H, O'Neill PL, Price C, Suomi SJ 1993. Old, socially housed rhesus monkeys manipulate objects. Zoo Biology 12, 285-298
"More than 10% of the [group-housed] females' time was spent in object [toy] manipulation. ... Socially housed rhesus monkeys ranging in age from 14 to 22 years showed steady rates of object manipulation, and their interest in familiar objects did not appear to wane over time. .... Several factors [for interpreting higher interaction rates in groups-housed than in single-housed animals] should be considered, the first of which is social facilitation ... Failure to manipulate objects in rhesus macaques appears to be more a function of individual housing than of old age."

Paquette D, Prescott J 1988. Use of novel objects to enhance environments of captive chimpanzees. Zoo Biology 7, 15-23
"Following their familiarization with the novel objects [rubber or plastic toys for small children], the [group-housed] chimpanzees' manipulation frequency decreased whereas self-grooming and abnormal behaviors were increased." The importance of a periodical substitution of the objects was suggested to enhance their usefulness.

Plesker R, Heller-Schmidth J, Hackbarth H 2006. Environmental enrichment objects for the improvement of locomotion of caged rhesus macaques (Macaca mulatta). Laboratory Primate Newsletter 45(1), 7-10
Juveniles used the mobile objects [treadmill and rotating barrel] more than the adults. "Due to the increase in locomotion, the amount of time spent in aggressive behavior significantly decreased."

Pruetz JD, Bloomsmith MA 1992. Comparing two manipulable objects as enrichment for captive chimpanzees. Animal Welfare 1, 127-137
"Paper was used a mean 27 per cent of the available time [one hour], while the Kong Toys were used a mean 10 per cent of the available time. ... Object use steadily declined over the first hour of exposure. ... Object use when the Kong Toy was present declined over the course of the study, but use of the paper remained consistent. ... The destructible wrapping paper was more worthwhile enrichment object than the indestructible Kong Toy for the [group-housed] captive chimpanzees of this study."

Shefferly N, Fritz J, Howell S 1993. Toys as environmental enrichment for captive juvenile chimpanzees (Pan troglodytes). Laboratory Primate Newsletter 32(2), 7-9
"Whereas contact with the indestructible toy ball decreased over time, destructible objects maintained a consistent level of interest throughout the toys lifespan. ... Provision of both types of toys did not result in significant differences in the time individuals spent in abnormal, or aggressive behavior. ... There were no health problems or injuries associated with the destructible objects. No pieces of plastic were found in feces, indicating that none had been ingested."

Weick BG, Perkins SE, Burnett DE, Rice TR, Staley EC 1991. Environmental enrichment objects and singly housed rhesus monkeys: Individual preferences and the restoration of novelty. Contemporary Topics in Laboratory Animal Science 30(5), 18
"We found that the extent of physical contact with the [Kong toy, Nylabone ring and Nylabone ball] toys habituated during a short time. ... The introduction of a different toy every Monday was accompanied by a restoration of the apparent novelty of the toys."

(6,2) Wooden Objects

*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 4.10. Wooden Objects. Washington, DC: Animal Welfare Institute
"I give our single-caged baboons 20 cm long gnawing sticks made of pecan branches. They love them! It takes one to two weeks for a stick to be "widdled" down to about half of its size."

Eckert K, Niemeyer C, Anonymous , Rogers RW, Seier J, Ingersoll B, Barklay L, Brinkman C, Oliver S, Buckmaster C, Knowles L, Pyle S 2000. Wooden objects for enrichment: A discussion. Laboratory Primate Newsletter 39(3), 1-4
"It seems that there is a general consensus that wooden objects provide inexpensive, safe, long-term and effective stimulation for the expression of non-injurious, species-typical behaviors such as perching, gnawing, gouging, manipulating and playing" without causing health and hygienic problems.

Hienz RD, Zarcone TJ, Turkkan JS, Pyle DA, Adams RJ 1998. Measurement of enrichment device use and preference in singly caged baboons. Laboratory Primate Newsletter 37(3), 6-10
"Baboons generally interacted less with Kongs than with logs or swings. This trend, however, was not consistent for each individual animal. Of the six baboons, three clearly "preferred" the log (i.e., moved the log more than the other two devices), two preferred the swing, and one preferred the Kong. Thus the trends expressed in the averaged data can be quite misleading."

Hienz RD, Pyle DA, Frey JJ, Zarcone TJ, Adams RJ, Turkkan JS 2000. Enrichment device use by baboons during long-term vs. intermittent availability. Laboratory Primate Newsletter 39(2), 1-3
"Four of the six baboons increased their [cherry] log use over the exposure period [104 days], while the remaining two baboons decreased their interactions with their logs over this period. ...When the logs were available only every other day, or every fourth day, log use was considerably enhanced on those days. When the logs were withheld longer, log use declined to the same level of use observed when the logs were continuously available. These results suggest that leaving enrichment devices out of a monkey's cage for extended periods would not be beneficial for generating greater use."

Hienz RD, Jones A, Pyle DA, Johnson J 2002. Effectiveness of enrichment devices during brief periods of social restriction in singly housed baboons. Laboratory Primate Newsletter 41(3), 1-3
"Data were collected on the animals' (three singly caged adult males) daily biscuit intake and activity levels as well as log activity prior to, during, and following social restriction (housed in separate room in which no other animals are present), and also in the absence and presence of a log (hand-cut cherry hardwood logs; 9 cm diameter x 35 cm long). .. All three baboons in the current study showed a marked decrease in activity during the brief periods of social restriction when the log enrichment devices were not available. However, once these devices were provided, general activity increased again, with two of the three baboons increasing their activity levels to near-normal. .. These findings present further support for the importance of enrichment devices for laboratory primates, showing that in the presence of such devices, the behavior of the animal is positively influenced. While the devices themselves were not manipulated greatly in this study, their presence affected the activity of the baboons."

Line SW, Morgan KN 1991. The effects of two novel objects on the behaviour of singly caged adult rhesus macaques. Laboratory Animal Science 41, 365-369
Single-housed subjects engaged in stick use 5.8% of 15 minute-observation sessions. The corresponding figure for nylon ball use was 2%. "No adverse health effects of stick ingestion were noted among the subjects."

Reinhardt V 1990. Time budget of caged rhesus monkeys exposed to a companion, a PVC perch and a piece of wood for an extended time. American Journal of Primatology 20, 51-56
"Sixty animals were continuously exposed for at least 1.5 years to a compatible companion for social interaction, a suspended plastic pipe for perching, and a branch segment for gnawing." Individuals spent an average of 23.5% of the time interacting with the companion, 10.4% with the plastic pipe and 4.8% with the branch segment.

Reinhardt V 1997. The Wisconsin Gnawing Stick. Animal Welfare Information Center (AWIC) Newsletter 7(3-4), 11-12
The sticks consist of branch segments cut of dead red oak trees. They are used by caged macaques about 5% of the time - more by young animals, less by adult animals - for gnawing, manipulating and playing. "All caged rhesus macaques (more than 700 animals) and all caged stumptailed macaques (approximately 36 animals) have continual access to gnawing sticks since that time [1989]. ... Long-term exposure to the sticks has resulted in no recognizable health hazards."

(6,3) Mirrors

*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 4.5. Mirrors. Washington, DC: Animal Welfare Institute
"All of our single-housed long-tailed macaques have mirrors mounted on swivels that are attached to the outside of their cages, low enough so that an animal can chose to either bend down and intentionally look into the mirror or to make no extra effort, hence not be confronted bothered? by the mirror reflection. Our monkeys use their mirrors frequently.
Our rhesus love mirrors too. They like to check us out by looking at us through the mirror. I guess they don't feel so threatened when they can look at us without being seen. They also like to check out the room, by looking at the reflections in the mirror. We have one male who never looks at people directly, but holds up a polished stainless steel mirror to watch people who have just entered the room. Of course, we named him Mirror Man.
We have found an acrylic sheet mirror that we can cut into different-size pieces. Some get hung on the walls, using double sided tape, while other pieces get hung right inside the enclosures, using zip ties. We also cut small pieces and give these directly to the primates. Our rhesus macaques often combine the wall and hand mirrors to get extra viewing advantage! It's really fun to watch them. The acrylic leaves no sharp edges when it breaks; this means it is safe for the animals. We never encountered a problem.
Our singly housed baboons get the most enjoyment from their mirrors, while pair- and group-housed animals show little interest in them.
I have a male olive baboon in my charge who regularly sits for long periods at a time looking at himself in a mirror. He is housed with two females but appears to prefer looking at his own mirror reflection versus the nice tumescent females hovering around him! He also uses his mirror to see reflections of what is going on behind him, sitting diagonally with his back facing the main traffic area for techs, as if he was spying on us! I do believe he is entertaining himself quite a bit with the mirror."

Brent L, Stone AM 1996. Long-term use of television, balls, and mirrors as enrichment for paired and singly caged chimpanzees. American Journal of Primatology 39, 139-145
"Chimpanzees used televisions, balls, and mirrors for 0.27-1.53% of the observation time after several years of exposure to the enrichment items. Television and ball use were significantly higher than mirror use."

Goode TL, McPherson H, Hughes J, Conboy T, Smith S, Bone A, Zimmerman W, Holder D, Klein H 1998. Evaluation of stainless steel reflective discs as enrichment devices for rhesus monkeys (Macaca mulatta) housed in a toxicological facility. Contemporary Topics in Laboratory Animal Science 37, 100
"The enrichment device was used [probably by single-caged subjects] primarily for manipulation and banging. ... The usage of polished stainless steel discs declines over time and therefore alternative methods of environmental enrichment and rotation of enrichment devices should be considered."

Harris H 2002. Mirrors as enrichment for monkeys. Laboratory Animal Refinement and Enrichment Forum (electronic discussion group), November 13, 2002
"Our African green monkeys (all males) and cynomolgus macaques use the mirrors more than the rhesus and squirrel monkeys. .. The mirrors are utilized by singly-caged, paired and group housed monkeys. They use them to look at themselves and at other things inside and outside the room. We have had a few (less than 10) occurrences where the monkeys were too fearful or self-aggressive to keep a mirror on their cage, but by far, the majority benefit from them. The mirrors, in my opinion, are one of our most useful object enrichment items."

O'Neill PL, Wright AC, Weed JL 1997. Curious response of three monkey species to mirrors. American Zoo and Aquarium Association (AZA) Regional Conference Proceedings, 95-101
One mirror was hung on the front of each subject's cage and remained in place for a two-week study period. Pig-tailed macaques contacted the mirror at a fairly constant rate of 12-18 times per hour. Rhesus macaques were initially interested in the mirror, but contact rate per hour progressively dropped to only 6 at the end of the second week. Long-tailed macaques showed little interest in the beginning, but contact rates reached those of pig-tailed macaques at the end of the study.

(7) Promoting Curiosity Behavior

(7,1) Television and Videos

Bloomsmith MA, Lambeth SP 2000. Videotapes as enrichment for captive chimpanzees (Pan troglodytes). Zoo Biology 19, 541-551
"Individually housed subjects watched the videotapes more than socially housed subjects. When viewing time was averaged across all videotapes, the chimpanzees watched the monitor a mean of 38.4% of the time available. ... Subjects habituated to repeated presentations of the videotapes, although the effect was small numerically. Although this type of enrichment did not extensively alter behavior, it did occupy a significant portion of the subjects activity budget."

Bloomsmith MA, Lambeth SP, Perlamn JE, Hook MA, Schapiro SJ 2000. Control over videotape enrichment for socially housed chimpanzees. American Journal of Primatology 51, Supplement 1, 44-45
Social behavior and solitary play were higher in subjects with control over the onset of videotapes, while scratching [generally regarded as a sign of tension] was higher in those groups who lacked control. "The results indicate that giving chimpanzees control over videotaped enrichment had limited, but positive, effects on behavior."

Harris LD, Briand EJ, Orth R, Galbicka G 1999. Assessing the value of television as environmental enrichment for individually housed rhesus monkeys: A behavioral economic approach. Contemporary Topics in Laboratory Animal Science 38(2), 48-53
"The negative demand curve suggested that TV is not a valued commodity" for single-caged rhesus macaques.

Lambeth S, Bloomsmith M, Baker K, Perlman J, Hook M, Schapiro S 2001. Control over videotape enrichment for socially housed chimpanzees: Subsequent challenge tests. American Journal of Primatology 54(Supplement 1), 62-63
"The lower expression of stressrelated behaviors by chimpanzees that took advantage of the opportunity to control the videotape apparatus implies that exerting control over the environment may have a generalized effect by lessening disturbance caused by mildly challenging situations."

O'Neill-Wagner P 2001. Videotape exposure may facilitate recovery for monkeys in a clinical setting. American Journal of Primatology 54(Supplement 1), 59
"During videotape exposure monkeys did not remove their sutures. Animals that had previously withdrawn from food were observed eating during videotapes showing primates eating."

Platt DM, Novak MA 1997. Videostimulation as enrichment for captive rhesus monkeys (Macaca mulatta). Applied Animal Behaviour Science 52, 139-155
The animals spent substantially more time watching selected videotapes than manipulating the joystick.

Plesker R, Herzog A 2001. Prima hedrons, puzzle feeders and television as environmental enrichment for captive African Green Monkeys. Primate Eye, 4
"The access to television (mainly nature films) enhanced the observation behaviour of the whole group for a short time. Again, the adult males, but also the youngest offspring did not appear to be interested."

Rumbaugh DM, Washburn DA, Savage-Rumbaugh ES 1989. On the care of captive chimpanzees: Methods of enrichment. In Housing, Care and Psychological Wellbeing of Captive and Laboratory Primates Segal EF (ed), 357-375. Noyes Publications, Park Ridge
"Television can be a great source of environmental enrichment if the chimpanzee can perceive the relevance of what it sees on the screen to the world it knows."

(7,2) Windows

*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 4.7. Windows. Washington, DC: Animal Welfare Institute
"We expose our squirrel monkeys to natural daylight via big windows during the summer. This is supplemented with artificial light in late fall and early spring, when the days are short, and throughout the winter. Some of our squirrel monkeys will lie as close to the window as possible and let the sun rays dance on their belly.
I've seen the same behavior in our marmosets. As soon as the sunlight hits the window, the animals stop what they are doing, run over to the window ledge, and start stretching out and basking in the sunrays. There is no doubt in my mind that exposure to natural light, especially sunlight, is highly appreciated by the animals.
All our rhesus macaques have access to one-way glass exterior windows mounted high above ground level. I very often see the animals gather up, attentively gazing out of the windows towards the source of some noise, at caretakers, activities in the garden and birds. One would think that exposure to daylight and the natural diurnal rhythm couldn't be anything else but a good thing for these animals."

Lynch R, Baker D 2000. Primate Enrichment: A room with a view. Laboratory Primate Newsletter 39(1), 12
Pairs were transferred to a play room with windows for 1½ hours every ten days. "During the past year, we have observed that the primates spend about an hour of their time looking out the windows."

(8) Safety Concerns

Eckert K, Niemeyer C, Anonymous , Rogers RW, Seier J, Ingersoll B, Barklay L, Brinkman C, Oliver S, Buckmaster C, Knowles L, Pyle S 2000. Wooden objects for enrichment: A discussion. Laboratory Primate Newsletter 39(3), 1-4
"It seems that there is a general consensus that wooden objects provide inexpensive, safe, long-term and effective stimulation for the expression of non-injurious, species-typical behaviors such as perching, gnawing, gouging, manipulating and playing" without causing health and hygienic problems.

Etheridge MA, O'Malley J 1996. Diarrhea and peritonitis due to traumatic perforation of the stomach in a rhesus macaque (hardware disease). Contemporary Topics in Laboratory Animal Science 35(5), 57-78
"Abdominal radiographic views indicated ingestion of approximately 20 pieces of wire that came from an old automobile tire hung in the outdoor monkey pen to provide environmental enrichment."

Hahn NE, Lau D, Eckert K, Markowitz H 2000. Environmental enrichment-related injury in a macaque (Macaca fascicularis): Intestinal linear foreign body. Comparative Medicine 50, 556-558
"As a result of this incidence [ingested sisal rope pieces leading to multiple ulcerations, perforations, septic peritonitis] sisal rope enrichment devices were immediately removed from all macaque cages in the facility."

Mahoney CJ 1992. Some thoughts on psychological enrichment. Lab Animal 21(5), 27,29,32-37
"Facilities must exercise caution when installing such climbing devices as vertically hanging or horizontally suspended ropes and chains - these must not crisscross or be too slack, because an animal can strangle its neck, limbs, or other body parts."

Murchison MA 1993. Potential animal hazard with ring toys. Laboratory Primate Newsletter 32(1), 1-2
"Recently one animal, a 2-year-old pigtail macaque (Macaca nemestrina), approximate weight 3.1 kg, became trapped inside a Nylaring. The ring went around the neck, across the body, and under one arm. Since the animal was apparently unable to remove the ring, he was anesthetized and the ring manually removed."

Novak MA, Rulf A, Munroe H, Parks K, Price C, O'Neill PL, Suomi SJ 1995. Using a standard to evaluate the effects of environmental enrichment. Lab Animal 24(6), 37-42
Monkeys maintained on pine wood shavings for a long period of time showed an increase in agonism, scratch, and stereotypy.

Reinhardt V 1997. The Wisconsin Gnawing Stick. Animal Welfare Information Center (AWIC) Newsletter 7(3-4), 11-12
"All caged rhesus macaques (more than 700 animals) and all caged stumptailed macaques (approximately 36 animals) have continual access to gnawing sticks since that time [1989]. ... Long-term exposure to the sticks has resulted in no recognizable health hazards."

Shefferly N, Fritz J, Howell S 1993. Toys as environmental enrichment for captive juvenile chimpanzees (Pan troglodytes). Laboratory Primate Newsletter 32(2), 7-9
"Whereas contact with the indestructible toy ball decreased over time, destructible objects maintained a consistent level of interest throughout the toys lifespan. ... There were no health problems or injuries associated with the destructible objects. No pieces of plastic were found in feces, indicating that none had been ingested."

Tresz H 1997. Providing enrichment at no cost. The Shape of Enrichment 6(4), 1-4
"Green pine cones can cause severe diarrhea. Keepers should work only with old, opened-up pinecones."

Regulations and Guidelines

American Society of Primatologists 2000. American Society of Primatologists guidelines for the ethical treatment of nonhuman primates. ASP Bulletin 24(4), 4
"ASP members hold the following general principles in common:
1. The most important of these principles is that we accept the responsibility of stewardship for nonhuman primates, and this responsibility must [sic] be reflected in our husbandry practices and research protocols whether in field, laboratory, or other setting.
3. Research with nonhuman primates should avoid pain and distress at every opportunity.
5. We should make use of information on a species natural history to improve management and enrich environments, because physical and psychological well-being are essential not only to the health of the animals but also to the validity of the research results.
6. Finally, we recognize that our concern should be extended to nonhuman primates once they have become 'surplus' to our research needs. This obligation entails ensuring quality care to the end of their natural lives whenever possible. .. While recognizing that some professional believe euthanasia is an acceptable way to deal with surplus animals in some cases, we strongly urge that other solutions be found whenever possible."

Canadian Council on Animal Care 1984. Chapter XX: Non-human primates. In Guide to the Care and Use of Experimental Animals, Volume 2 Canadian Council on Animal Care (ed), 163-173. Canadian Council on Animal Care, Ottawa, Canada "Any primate housed alone will probably suffer from social deprivation, the stress from which may distort processes, both physiological and behavioural."

Canadian Council on Animal Care 1993. Guide to the Care and Use of Experimental Animals, Volume 1, 2nd Edition. Canadian Council on Animal Care, Ottawa, Canada
"All animals must be observed at least once daily. .. The social needs of animals used in research, teaching, or testing, should be given equal consideration with environmental factors such as lighting, heating, ventilations and containment (caging). Particularly in the case of singly housed animals, daily observation provides an alternative from of social contact for the animal and commonly facilitates handling in that the animal becomes accustomed to the human presence. .. Most animals should not be housed singly unless required by medical condition, aggression, or dictates of the study. Singly housed animals should have some degree of social contact with others of their own kind. .. In the interest of well-being, a social environment is desired for each animal which will allow basic social contacts and positive social relationships. Social behaviour assists animals to cope with circumstances of confinment. .. Restraint procedures should only be invoked after all other less stressful procedures have been rejected as alternatives. ... Physiological, biochemical and hormonal changes occur in any restraint animal ... and investigators should consider how these effects will influence their proposed experiments."

*Council of Europe 2006 Appendix A of the European Convention for the Protection of Vertebrate Animals Used for Experimental and Other Scientific Purposes (ETS No. 123) enacted June 15, 2007. Strasbourg, France: Council of Europe
Progressive regulations pertaining to the species-appropriate housing and handling of animals kept in research labs.
"Because the common laboratory non-human primates are social animals, they should be housed with one or more compatible conspecifics. .. Single housing should only occur if there is justification on veterinary or welfare ground. Single housing on experimental grounds should be determined in consultation with the animal technician and with the competent person charged with advisory duties in relation to the well-being of the animals.
Primates dislike being handled and are stressed by it; training animals to co-operate should be encouraged, as this will reduce the stress otherwise caused by handling. Training the animals is a most important aspect of husbandry, particularly in long-term studies. .. Training can often be employed to encourage the animals to accept minor interventions, such as blood sampling.
The flight reaction of non-human primates from terrestrial predators is vertical, rather than horizontal; even the least arboreal species seek refuge in trees or on cliff faces. As a result, enclosure height should be adequate to allow the animal to perch at a sufficiently high level for it to feel secure. .. The minimum enclosure height for caged marmosets and tamarins is 1.5 m; the minimum enclosure height for caged squirrel monkeys, macaques, vervets and baboons is 1.8 m. .. The structural division of space in primate enclosures is of paramount importance. It is essential that the animals should be able to utilise as much of the volume as possible because, being arboreal, they occupy a three-dimensional space. The make this possible, perches and climbing structures should be provided."

Home Office 1989. Animals (Scientific Procedures) Act 1986. Code of Practice for the Housing and Care of Animals Used in Scientific Procedures. Her Majesty's Stationery Office, London, UK
"Experimental results may be influenced by environmental conditions. .... Unstable environmental conditions are likely to introduce avoidable variability into biological responses. To demonstrate any experimental response against such a variable background generates a requirement for greater animal usage if the result is to be statistically valid. Good control of variables ... can therefore contribute both to good science and to the minimisation of animal use. .. The shape of the cage and the furniture provided may be as important to the animal as the overall size of the cage. ..All animals must be allowed to exercise. For the smaller species, this should usually be achieved by providing adequately sized cages or pens and sometimes play objects. ... For larger species, special arrangements will usually be required for social contact as well as exercise. ... The behaviour of an animal during a procedure depends on the confidence it has in its handler. This confidence is developed through regular human contact and, once established, should be preserved. .. Where appropriate, time should be set aside for handling and grooming. All staff, both scientific and technical, should be sympathetic, gentle and firm when dealing with animals. .. The least distressing method of handling is to train the animal to co-operate in routine procedures. Advantage should be taken of the animal's ability to learn."

Institute of Laboratory Animal Resources 1980. Laboratory Animal Management: Nonhuman Primates. National Academy Press, Washington, DC
"Lighting should be uniformly diffused throughout the area and provide adequate illumination for good house-keeping practices, adequate inspection of animals, and safe working conditions for personnel."

Institute for Laboratory Animal Research 1992. Recognition and alleviation of pain and distress in laboratory animals. National Academy Press, Washington, DC
"The purposes of this book are to increase awareness of the sources and manifestations of stress and distress in laboratory animals and to increase ethical sensitivity in those who use and care for them. (It might also, indirectly, help to reduce the number of animals needed for experimental purposes: uncontrolled pain or distress can increase variability in experimental data and so require the use of more animals in a study for it to achieve statistical significance.)
Stress is the effect produced by external (i.e., physical or environmental) events or internal (i.e., physiologic or psychologic) factors, referred to as stressors, which
induce an alteration in an animal's biologic equilibrium. ... Examples of potential stressors that cause psychologic stress [include] fear, anxiety, boredom, loneliness, separation.
Distress is an aversive state in which an animal is unable to adapt completely to stressors and the resulting stress and shows maladaptive behaviors" such as “coprophagy, hair-pulling, self-biting, and repetitive stereotyped movements. ... Such behaviors, like maladaptive ones, should be interpreted as causing harm to the animal and producing unwanted variability in research data. ... The identification and control of these [environmental] stressors from the animals' or species' perspective constitute good husbandry and are a primary responsibility of all who care for or use animals in a laboratory setting. ... Behavioral changes, however, are the earliest signs of stress or distress that most animal care staff and researchers are likely to confront. Skilled observers who know the behavior of a particular species or strain of animal and of the individual animals under their care could provide a reliable assessment of the state of the animals. That reliability is seriously compromised when few animal care staff and researchers are afforded the time or training necessary for them to become skilled observers. ... Recognition, or anticipation, that a particular event will be perceived as an important stressor by an animal requires knowledge not only of the stressor, but of the species-typical responses to situations and of the experience of the particular animal. ... Stroking and handling by humans can be a practical and effective technique for calming animals in situations where they are distressed, particularly animals that have been positively socialized by humans."

*International Primatological Society 2007 IPS International Guidelines for the Acquisition, Care and Breeding of Nonhuman Primates. Bronx, NY: International Primatological Society
"There is an acute need for the training of professional and technical personnel in veterinary care, psychological well-being, handling and general management of captive primates and the requirements of species and individuals. Well-trained, competent and motivated personnel can make an enormous difference in improving the welfare of captive primates.
Pair or group housing in an enclosure must be considered the norm for gregarious animals, but only compatible (socially, virological status, etc.) animals should be kept together. Infectious disease study does not necessarily preclude the ability to keep primates in pairs or groups in the same enclosure, without interfering with study validity. Many infectious disease studies are carried out in paired or grouped primates. the same is true of many other types of studies and procedures, such as pharmacokinetic studies and drug safety testing. .. Individual subjects can be accessed for testing and manipulation through good enclosure design, separation chutes and training using positive reinforcement techniques. .. For experimental animals, where housing in groups is not possible, keeping them in compatible pairs is a viable alternative social arrangement. Single caging should only be allowed where there is an approved protocol justification on veterinary or welfare grounds.
A two-tiered system is not recommended as these cages are usually too small. The lower tiers do not allow primates to engage in their vertical flight response, are often darker, and animals in the lower cages tend to receive less attention from attending personnel.
Adequate space alone does not in itself provide for good welfare, but larger enclosures allow greater complexity of cage furnishings and other enrichments, and greater flexibility for meeting social needs.
Illumination of each cage should be uniform and sufficient for adequate inspection of animals.
As animals like to work for their food, increasing processing time, increasing foraging, or providing puzzle feeders or other feeding devices is encouraged.
Infants should not be separated from their natal group at an early age but should remain with their mother until weaning age which varies greatly between species.
Primates of many species can be quickly trained using positive reinforcement techniques to cooperate with a wide range of scientific, veterinary and husbandry procedures. Such training is advocated whenever possible as a less stressful alternative to traditional methods using physical restraint. Techniques that reduce or eliminate adverse effects not only benefit animal welfare but can also enhance the quality of scientific research, since suffering in animals can result in physiological changes which are, at least, likely to increase variability in experimental data and, at worst, may even invalidate the research. Restraint procedures should be used only when less stressful alternatives are not feasible."

International Primatological Society 1993. IPS International guidelines for the acquisition, care and breeding of nonhuman primates, Codes of Practice 1-3. Primate Report 35, 3-29
Internationally accepted professional standards for the housing, handling of and environmental enrichment for nonhuman primates. "Size of enclosure is only of significance in terms of usable space and complexity within. .. The vertical dimension of the cage is of importance [because of the vertical flight response] and cages where the monkey is able to perch above human eye level are recommended. ... A compatible conspecific probably provides more appropriate stimulation to a captive primate than any other potential environmental enrichment factor. .. Monkeys should, unless there are compelling reasons for not doing so, be housed socially. ... Young monkey should not normally be separated from its mother at an early age (i.e., at 3-6 months) but should remain in contact for one year to 18 months, in most species. There is unlikely to be any greater productivity through early weaning, in seasonally breeding species, such as rhesus monkeys. Even in non-seasonal breeders, any slight increase in productivity must be offset against the resulting behavioural abnormalities of the offspring."

International Primatological Society 1989. IPS International Guidelines for the acquisition, care and breeding of nonhuman primates. Primate Report 25, 3-27
"Illumination should be uniform and sufficient for adequate inspection of animals and safe working conditions for personnel, but not obtrusive to the well-being of the animals. .. Restraint procedures should be used only when less stressful alternatives are not feasible. .. Primates of many species can be trained for sample procedures, such as presenting a limb for a blood collection, and such training is advocated whenever possible, using positive reinforcement."

Medical Research Council 2004. MRC Ethics Guide: Best Practice in the Accomodation and Care of Primates used in Scientific Research. Medical Research Council, London, UK
"Primates must [sic] be provided with a complex and stimulating environment that promotes good health and psychological well-being and provides full [sic] opportunity for social interactions, exercise and to express a range of behaviours appropriate to the species. .. The volume and height of the cage (or enclosure) are particularly important for macaques and marmosets, which flee upwards when alarmed. Their cages and enclosures should be floor-to-ceiling high whenever possible, allowing the animals to move up to heights where they feel secure. Double-tiered cages should not be used since they restrict the amount of vertical space available to the animals. Special justification should be given for using cages with grid floors (eg, compelling scientific or veterinary reasons) as this restricts the opportunity to provide substrate and forage. In the case of macaques, cages should be linked to a play area or enclosure .. They should have unlimited access to this area unless it is necessary to confine them for scientific, husbandry, veterinary or welfare purposes. Where security permits, the accommodation should have natural light. .. Primates should be socially housed as compatible pairs or groups, depending on their age and sex and the nature of the scientific procedures or study. .. Primates should not be singly housed unless there is exceptional scientific or veterinary justification. .. Cages and enclosures should be furnished to encourage primates to express their full [sic] range of behaviours. Depending on the species, this should normally include provision for resting, running, climbing, leaping and foraging. ..Shelves, ladders and branches should be made from wood wherever possible even though they will have to be replaced more often. .. The cage and enclosure should provide the animals with an area of privacy. .. To help prevent boredom, novelty should be regularly introduced into the environment, for example, by re-arranging some of the cage furniture. .. The MRC will require justification for the use of scientific procedures that restrict the opportunity to forage. .. Positive reinforcement techniques should be used to train primates to cooperate with catching, handling, restraint and research procedures. The routine use of squeeze-back cages and nets should be actively discouraged."

National Center for the Replacement, Refinement and Reduction of Animals in Research. 2006 Non-human Primates. London: National Center for the Replacement, Refinement and Reduction of Animals in Research
"Basic requirements for good primate housing include the following: Housing in stable, compatible groups (pairs at least); enough space for exercise, a range of normal behaviours and suitable enrichment; solid floors with substrate; sufficient enclosure height to allow vertical flight if alarmed; no double tiers; climbing structures to increase useable space (perches, platforms, swings, ropes, ladders); sufficient for all animals to occupy simultaneously; a varied diet appropriate for the species; the ability to forage, including appropriate artificial feeding devices and scatter feeding; adequate light levels; access to outdoors wherever possible; nest boxes for species that use them, e.g. marmosets; wood for gnawing and scent-marking for species that use it, e.g. marmosets; visual barriers for control over social interactions; toys, chews, tactile materials, destructible materials to provide a degree of control over the environment; novelty - minor changes in furniture, feeding practices, toys; Adequate socialization and habituation to humans, and training where appropriate."

National Center for the Replacement, Refinement and Reduction of Animals in Research. 2006 NC3Rs Guidelines: Primate Accomodation, Care and Use. London: National Center for the Replacement, Refinement and Reduction of Animals in Research
"The guidelines were developed by reviewing the published literature and through consultation with the scientific community, veterinary and animal care staff, the Animals (Scientific Procedures) Inspectorate, and animal welfare organisations. They represent a framework for applying and reviewing the expectations of the funding bodies in the humane [sic] use of primates. The guidelines set out contemporary best practice in the use of primates in biomedical, biological, veterinary and behavioural research, and include principles relating to the source, housing, capture, handling, restraint and training of primates. .. They are readily applicable to the majority of research programmes using primates. .. Cages and enclosures should be floor to ceiling high whenever possible, with adequate perching to allow all animals to move up to heights where they feel more secure. .. Double-tiered cages should not be used since they restrict the amount of vertical space available to the animals. .. Where security permits, the accomodation should have natural light. .. Primates should be socially-housed as compatible pairs or groups. .. Primates should not be housed singly unless there is exceptional [sic] scientific or veterinary justification. .. The vertical and horizontal dimensions of the cage and enclosure should be exploited fully by incorporating shelves, logs, ladders, climbing structures, branches, hammocks, swings, ropes and objects to manipulate. .. Shelves, ladders and branches should be made from wood wherever possible. .. All primates should be given the opportunity to forage daily, by scattering food in litter or substrate on the floor, or in a tray, and by using devices that encourage foraging activity. .. Positive reinforcement techniques should be used to train primates to cooperate with capture, handling, restraint and research procedures. The routine use of squeeze-back cages and nets should be actively discouraged."

National Health and Medical Research Council 2004. Australian Code of Practice for the Care and Use of Animals for Scientific Purposes 7th Edition. Australian Government Publishing Service, Canberra, Australia
"People who use animals for scientific purposes have an obligation to treat them with respect and consider their welfare as an essential factor when planning and conducting studies."

National Health and Medical Research Council [NHMRC] Animal Welfare Committee 2003. Policy on the Use of Non-Human Primates in Medical Research. National Health and Medical Research Council, Canberra, Australia
"Social interaction is paramount for well-being. Social deprivation in all its forms must be avoided. ... Animals that need to be individually caged, either for experimental or holding purpose (for example, aggressive adult males), must be given contact with conspecific animals. ... Accomodation should provide an environment which is as varied as possible. It should meet the behavioural requirements of the species being used and must provide access to an outside enclosure for animals held long-term (that is, longer than six weeks). ... Emphasis must be placed on environmental enrichment."

National Research Council 1996. Guide for the Care and Use of Laboratory Animals, 7th Edition. National Academy Press, Washington, DC
"Proper care, use, and humane treatment of animals used in research, testing, and education .. require scientific and professional judgment based on knowledge of the needs of the animals. .. A good management program provides the environment, housing, and care that ... minimizes variations that can affect research. .. Animals should be housed with the goal of maximizing species-specific behaviors and minimizing stress-induced behaviors. For social species, this normally requires housing in compatible pairs or groups. .. In general, lighting should be diffused throughout an animal holding area and provide sufficient illumination for the well-being of the animals and to allow good housekeeping practices, adequate inspection of animals - including the bottom-most cages in racks - and safe working conditions for personnel."

National Research Council 1998. The Psychological Well-Being of Nonhuman Primates. National Academy Press, Washington, DC
Meeting the criteria of psychological well-being implies:
· "Appropriate social companionship.
· Opportunities to engage in behavior related to foraging, exploration, and other activities appropriate to the species, age, sex, and condition of the animal.
· Housing that permits suitable postural and locomotor expression.
· Interactions with personnel that are generally positive and not a source of unnecessary stress.
Procedures that reduce reliance on forced restraint ... are less stressful for animals and staff, safer for both, and generally more efficient. .. Social interactions are considered to be one of the most important factors influencing the psychological well-being of most nonhuman primates. ... Knowing that most primates benefit from social interactions, it should be obvious tht they can be harmed by a lack of social interaction. .. The common practice of housing rhesus monkeys singly calls for special attention. .. Every effort should be made to house these [singly caged] animals socially (in groups or pairs), but when this is not possible, the need for single housing should be documented by investigators and approved by the IACUC. ... Although the causes of self-directed biting are poorly understood, prolonged individual housing is probably an influential contributing factor.
... To reduce the stress of physical restraint, many primates can be trained for routine procedures. ... Under natural conditions, many primates spend much of their lives aboveground and escape upward to avoid terrestrial threats. Therefore, these animals might perceive the presence of humans above them as particularly threatening .. Even macaques, which some describe as semiterrestrial, spend most of the day in elevated locations and seek the refuge of trees at night ..Optimal use of available cage space might well depend more on the placement of perches, platforms, moving and stationary supports, and refuges than on cage size itself. .. The animal technician's and caregiver's roles are pivotal to the social support of primates, particularly animals that are singly caged. .. Enrichment methods that have not been subjected to empirical testing should be viewed simply as invalidated ideas, regardless of how well intended they might be."

Office of Laboratory Animal Welfare (OLAW) 2006 Enrichment for Nonhuman Primates. Bethesda, MD: Office of Laboratory Animal Welfare
"This book serves as an introduction to the basic behavior and environmental enrichment." In baboons "boredom, stress and, ultimately, problem behavior may result from confinement in small enclosures, lack of enrichment activities, solitary housing ... Examples of abnormal behavior patterns .... are hair eating and regurgitation. .. More severe problems, such as self-biting, also have been reported in captive baboons. ... Captive chimpanzees may develop bad habits, including strange behaviors not normally seen in the wild. [e.g. hair plucking] ... Diarrhea may be a response to psychological stress. ... Because of the intrinsic social nature of macaques, pair or group housing of compatible animals is extremely important. ... Because of the animals' [macaques] tendency to flee upward when escaping a perceived threat, they benefit from perches, shelves or other structures that increase the three-dimensional space of the enclosure. Generally, older macaques prefer a non-moving shelf or perch, while the younger ones will readily use swings. ... Because the monkeys will chew on these toys, they should be relatively durable, such as heavy-duty dog toys. ... Rotating different toys in the enclosure and removing them periodically will help to keep the toys novel and increase the animals' interest in them. ... Abnormal behaviors are an undesirable consequence of captive housing, reflecting an inadequate environment for maintaining the animal. ... Redirection of an abnormal behavior [e.g., via fleece etc.] is not a 'cure' and should only be regarded as a temporary correction." ... "Self-injurious behaviors" ... "such as self hair-pulling and self-biting, often are the result of unusual stress". They also occur in squirrel monkeys where "'pacing' may be eliminated by increasing the animal's available travel paths by installing additional perches."

Organisation for Economic Co-Operation and Development [OECD] 2000. Guidance Document on the Recognition, Assessment, and Use of Clincal Signs as Humane Endpoints for Experimental Animals Used in Safety Evaluation [OECD Guidance Document No. 19 on Humane Endpoints]. OECD, Paris, France
"A humane endoint can be defined as the earliest indicator in an animal experiment of severe pain, severe distress, suffering, or impending death. .. Pain can be defined as an upleasant sensory and emotional experience associated with actual or potential tissue damage, or described in terms of such damage." Distress is "An aversive state resulting from maladaption or inability to adapt to stressors. .. Distress is usually associated with a change in motility or locomotion, and can result in stereotype behaviour. .. Retreat to a corner of the cage or excessive struggling or vocalisation on dosing are examples of distress in anticipation of an experimental procedure. .. If something is known to cause suffering in humans, it should be assumed to cause suffering in animals."

Prentice ED, Zucker IH, Jameton A 1986. Ethics of animal welfare in research: The institution's attempt to achieve appropriate social balance. The Physiologist 29, 1&19-21
"Physical restraint procedures should be used on awake animals only after alternative procedures have been considered and found to be inadequate. If a restraint will be utilized the animal should be trained or conditioned to the restraining device, using positive reinforcement, prior to the beginning of the experiment"

Public Health Service (PHS) 1996. U.S. Government Principles for the Utilization and Care of Vertebrate Animals Used in Testing, Research, and Training. In Guide for the Care and Use of Laboratory Animals National Research Council 117-118. National Academy Press, Washington, DC
"Unless the contrary is established, investigators should consider that procedures that cause pain or distress in human beings may cause pain or distress in other animals."

Smith JA, Boyd KMe 2003. The Boyd Group of papers on: The use of non-human primates in research and testing. Animal Technology and Welfare 2, 89-97
"Unless specifically justified, infants should remain with their mothers until they are no longer dependent on them. .. The minimum cage sizes for both marmosets and macaques detailed in the Home Office guidance (1989), and the European standards, are inadequate - particularly in respect of vertical dimensions of cages - and do not reflect current best practices. ... Every effort should be made to train non-human primates to accept routine scientific procedures, and so minimise the stress caused to the animals."

USDA 2002. Animal Welfare Regulations Revised as of January 1, 2002 [Code of Federal Regulations, Title 9, Chapter 1, Parts 1-4 United States Department of Agriculture]. U.S. Government Printing Office, Washington
"Handling of all animals shall be done as expeditiously and carefully as possible in a manner that does not cause trauma, overheating, excessive cooling, behavioral stress, physical harm, or unnecessary discomfort. ... Deprivation of food or water shall not be used to train, work, or otherwise handle animals. .. Lighting must be uniformly diffused throughout animal facilities and provide sufficient illumination to aid in maintaining good housekeeping practices, adequate cleaning, adequate inspection for animals, and for the well-being of the animals. .. Inadequate space may be indicated by ... stress, or abnormal behavior patterns. .. Primary enclosures .. must [sic] provide sufficient space for the nonhuman primates to make normal postural adjustments with freedom of movement. .. These minimum space requirements must [sic] be met even if perches and ledges, swings, or other suspended fixtures are placed in the enclosure. .. Research facilities must [sic] develop, document, and follow an appropriate plan for environmental enhancement. .. The plan must [sic] include specific provisions to address the social needs of nonhuman primates. .. The physical environment in the primary enclosures must be enriched by providing means of expressing species-typical activities."

Working Party for the Preparation of the Fourth Multilateral Consultation of Parties to the European Convention for the Protection of Vertebrate Animals Used for Experimental and Other Scientific Purposes (ETS 123) 2000. Proposal II (General part of Appendix A). Council of Europe, Strasbourg, France
"Consideration should be given to windows, since they are a source of natural light and can provide environmental enrichment for some species, especially primates. ...Animals should be socially housed whenever possible and provided with an adequately complex environment within the enclosures to enable them to carry out a range of normal behaviours. Restricted environments can lead to behavioural and physiological abnormalities and affect the validity of scientific data. ... Unless otherwise specified, additional surface areas provided by cage inserts such as shelves should be provided in addition to the recommended minimum floor areas. .. The flooring should provide a solid, comfortable resting area for all animals. .. Animal care staff are expected, at all times, to have caring and respectful attitude towards animals in their care, and to be proficient in their handling and restraint. .. Where appropriate, staff time should be set aside for talking, handling and grooming."

Zimmermann M 1987. Ethical principles for the maintenance and use of animal in neuroscience research. Neuroscience Letters 73, 1
"Animals are generally accepted to be sentient and capable of suffering, and to have species-specific requirements of living. ... Maintenance of experimental animals should account for species-specific needs of accommodation, activity, feeding and social interactions to the degree possible."

Surveys

Baker KC, Weed JL, Crockett CM, Bloomsmith MA 2007. Survey of environmental enhancement programs for laboratory primates. American Journal of Primatology 69, 377-394
"Here we report the results of a 2003 survey that was sent to individuals overseeing enrichment programs at a variety of primate research institutions. Data were obtained on the management of 35,863 primates in 22 facilities. While most primates were reported to be housed socially (73%), social housing for indoor-housed primates appears to have changed little over the past 10 years. Research protocol issues and social incompatibility were commonly cited constraints. Implementation of feeding, manipulanda, and structural enrichment was relatively unconstrained, and contributions to these aspects of behavioral management generally included individuals in a wide variety of positions within a facility. In contrast, enrichment devices were used on a less widespread basis within facilities, and positive reinforcement programs that involved dedicated trainers were rare."
"Social Housing: We focused on the indoor population to assess the current status of efforts to reduce the use of single housing in research. With outdoor-housed primates excluded from the analysis, our sample included 17,663 individuals, 46% of which were housed socially."
"Feeding Enrichment: All facilities included feeding enrichment in their plans. No facilities provided fewer than half (1-50%) of their nonhuman primates with feeding enrichment... Fruit was distributed at all facilities, nuts and seeds at 95%, vegetables at 91%, manufactured treats at 73%, and other items at 64% of facilities."
"Manipulanda: All facilities employed manipulable objects. Of the categories of manipulanda provided as response choices, the items used most frequently were mirrors (100%), balls (95%), synthetic chew toys (86%), and hanging toys (86%). Rattles were provided at 68% of the facilities, wood at 59%, and bells at 18%."
"Devices: Ninety-one percent of facilities reported the use of enrichment devices. Of the devices offered as response choices, the most common were puzzle tube feeders (77% of facilities) and Astroturf foraging boards (77%), followed by puzzle balls (59%), fleece boards (36%) and other devices (36%)."
"Structural Enrichment: Most facilities reported providing structural enrichment to all of their animals. All facilities reported the use pf perches, 73% swings, 59% used barrels, 50% bedding/nesting materials, 36% exercise cages or playrooms."
With respect to social housing, in the 1994 survey 38% of indoor-housed macaque species were housed socially. In the current survey, among these species, 44% of the individuals in cages wee housed socially. This comparison indicates that the use of social housing for caged primates has not expanded as substantially as many applied behavioral scientists would have hoped.
Since the practice of single housing is a major risk factor for the development of abnormal behavior, the continued prevalence of single housing perpetuates the need for intervention."

Bayne K 1989 Resolving issues of psychological well-being and management of laboratory nonhuman primates. In Housing, Care and Psychological Wellbeing of Captive and Laboratory Primates. Segal EF (ed), 27-39 . Noyes Publications, Park Ridge, NJ
"The survey indicated that approximately 83% of adult captive primates at NIH are caged alone. As only 9% of scientists interviewed currently train their animals to go into transport cages, the majority use squeeze panels to transfer animals or to restrain them at the front of the cage. ..The most frequent recommendations [of NIH scientists interviewed] were for larger and more complex cages."

Prescott MJ, Buchanan-Smith HM 2007. Training laboratory-housed non-human primates, part I: a UK survey. Animal Welfare 16(1), 21-36
Training using positive reinforcement is increasingly recognised as a valuable tool for the humane and effective management and use of laboratory-housed non-human primates. A survey was carried out on the use of training and other learning processes (socialisation, habituation and desensitisation) in over half of UK establishments using and breeding primates. There is widespread awareness of training as a refinement technique but it not used as widely or as fully as it might be. We conclude that there is opportunity for refinement of common scientific, veterinary and husbandry procedures (such as blood and urine collection, injection, capture from the group and weighing) through use of positive reinforcement training, especially when combined with appropriate socialisation, habituation and desensitation. Recommendations on best practice, training techniques and staff education are given.

Reinhardt V 1994. Survey of environmental enhancement for research macaques. Laboratory Primate Newsletter 33(3), 1-2
A survey of 11 facilities. The percentage of caged macaques permanently: a) exposed to enrichment objects ranged from 18% to 100% with a mean of 86%, b) housed in pairs or small groups ranged from 0% to 98% with a mean of 38%.

Ethical Considerations

Öbrink KJ, Rehbinder C 1999. Animal definition: a necessity for the validity of animal experiments? Laboratory Animals 22, 121-130
"'Material and Methods' section mostly reveals an obvious or almost total lack of information about the animals. ... If a researcher, through carelessness or ignorance, should use more animals for a project than is necessary, it must be considered unethical. ...Without hesitation, it is a scientific demand that all factors that have not proven to be insignificant should be checked, controlled or kept constant."

American Society of Primatologists 2000. American Society of Primatologists guidelines for the ethical treatment of nonhuman primates. ASP Bulletin 24(4), 4
"Despite their varied disciplines, ASP members hold the following general principles in common:
1. The most important of these principles is that we accept the responsibility of stewardship for nonhuman primates, and this responsibility must [emphasis added] be reflected in our husbandry practices and research protocols whether in field, laboratory, or other setting.
2. The number of nonhuman primates used in research should be the minimum required for valid research results.
3. Research with nonhuman primates should avoid pain and distress at every opportunity.
4. In all cases, the potential benefits of any research should be evaluated against the potential risks to their nonhuman primates subjects.
5. We should make use of information on a species natural history to improve management and enrich environments, because physical and psychological well-being are essential not only to the health of the animals but also to the validity of the research results.
6. Finally, we recognize that our concern should be extended to nonhuman primates once they have become 'surplus' to our research needs. This obligation entails ensuring quality care to the end of their natural lives whenever possible. .. While recognizing that some professional believe euthanasia is an acceptable way to deal with surplus animals in some cases, we strongly urge that other solutions be found whenever possible."

Arluke A 1994. The ethical socialization of animal researchers. Lab Animal 23(6), 30-35
"In all but two of the 35 laboratories, newcomers faced a closed moral universe where issues of morality were defined institutionally, and hence rarely confronted by individuals. ... It was controversial or risky to admit to having ethical concerns, because to do so was tantamount to admitting that there really was something morally wrong with animal experimentation, thereby giving 'ammunition to the enemy'."

Association of Veterinarians for Animal Rights 2005. Contemporary Veterinarian's Oath. Association of Veterinarians for Animal Rights, Davis, CA
"Being admitted to the profession of veterinary medicine,
I solemnly swear to use my scientific knowledge and skills to protect the health and well-being of all nonhuman animals, to relieve pain and suffering in nonhuman animals, to strengthen the understanding of the inherent needs and interests of all nonhuman animals, and to promote the preservation of wildlife and their natural environment.
I will practice my profession conscientiously, with dignity, compassion, and integrity.
I accept as a lifelong obligation the continual improvement of my professional knowledge and competence. "

*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 2.1. How to Refer to an AnimalUsing the Proper Pronoun. Washington, DC: Animal Welfare Institute
"As caregivers, we do not use the pronoun it when referring to an animal. An animal is not an object! We do not think that calling an animal he or she encourages anthropomorphism, but that it does acknowledge the fact that we are dealing with an individual sentient being who can feel discomfort, pain and distress in very similar ways as we do. Calling individual animals he or she helps us deal with something that deep down, we are not really comfortable with namely the fact that these animals have no choice about deciding whether they want to be used in research and then killed.
Referring to an animal as it is neither correct nor scientific, because it overlooks the fact that animals, just like humans, have a biological gender. Therefore, they should be referred to accordingly with the correct pronouns he or she. When we label an animal with the incorrect pronoun it, we risk treating the animal like an inanimate object incapable of feeling discomfort, pain and distress."

*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 2.2. Higher- Versus Lower-Order Species. Washington, DC: Animal Welfare Institute
"It seems that Refinement in the use of animals for research includes choosing lower-order species rather than higher-order species, presumably due to the assumption that the lower-order animals suffer less and that their use in experiments poses fewer ethical problems. Where do we draw the line?
For people who are using these terms, lower simply means less like humans, and higher means more like humans. This terminology is tied in with the incorrect view of evolution as a ladder of progress toward especially evolved beings, such as humans. How would animals, used by humans for biomedical research, classify the human species? Of a high order? Crown of creation? Very unlikely!
I think all animals deserve the same consideration, whether they are a rat or mouse of presumed low order or a dog or monkey of presumed higher order. It seems strange to me to categorize animals into different orders and then treat them accordingly."

Benn DM 1995. Innovations in research animal care. Journal of the American Veterinary Medical Association 205, 465-468
"Implementing enriched housing programs and policies assists the scientific community in meeting its ethical responsibilities toward the animals used in research."

Canadian Council on Animal Care, Olfert ED, Cross BM, McWilliam AA 1993. Guide to the Care and Use of Experimental Animals, Volume 1, 2nd Edition. Canadian Council on Animal Care, Ottawa
"We are morally responsible for any living thing that we cause to be dependent upon us, including animals used in research, teaching and testing."

Halpern-Lewis JG 1996. Understanding the emotional experiences of animal research personnel. Contemporary Topics in Laboratory Animal Science 35(6), 58-60
"Animal research personnel should be encouraged to join in the pursuit of progress with the recognition that, in addition to knowledge and skills, primary attributes must be feelings of compassion and sensitivity toward animals. Because animals cannot speak for themselves, it is up to empathetic and caring personnel to see that they are treated humanely and with respect. A variety of suggestions have been provided to enable research participants to perform necessary tasks without impeding experimental results or detracting from the integrity of the animal-human relationship. It is my belief that individuals who demonstrate caring behaviors while being allowed appropriate outlets for expression will remarkably enrich the overall research experience of humans and animals alike."

Herzog H 2002. Ethical aspects of relationships between humans and research animals. ILAR [Institute for Laboratory Animal Research] Journal 43(1), 27-32
"More often than not, moral dilemmas are the result of good people trying to do the right thing when the right thing is unclear. .. I have spoken with some animal care staff who have complained about investigators who rarely set foot in their institution's animal colony and who appear to regard research animals as organ repositories. In addition, some researchers show little understanding of the ethical problems faced by technicians. .. There is every reason to believe that individuals who care about their wards on a personal level actually treat the animals better. .. Inevitably, individuals who work with animals in the context of biomedical and behavioral research will sometimes form bonds with the animals with whom they interact. When an animal is transformed from `object' to `pet,' its moral status is changed. Although human-research animal relationships may enhance the well-being of laboratory animals, they involve a moral cost to the human caretakers. Institutions should acknowledge the existence of these bonds and provide support mechanisms to help laboratory personnel deal with the moral challenges of their profession."

Mroczek NS 1994. Recognizing animal suffering and pain. Lab Animal 23(1), 27-31
Highlights the "human conditioning to the incongruous position that considers animals dissimilar to humans with respect to drive, need, or sensation, yet similar enough to be used as models for the study of humans themselves. ... Identification, sympathy, and positive regard by a scientist or animal care worker can, most of all, help to encourage optimum care and treatment of animals in pain. Recognition of animals suffering and pain is made possible by feeling for and interest in animals themselves, as sentient organisms, first and foremost, and feeling for and interest in animal behavior in totality."

Petto AJ, Buchanan-Smith H 1994. Psychological well-being and other projections of the human condition: Their meaning for research activities with non-human primates. XVth Congress of the International Primatological Society, 359
"The often cited paradox for researchers studying nonhuman primates is that we must consider them sufficiently similar to us so that our studies will be valid and significant; at the same time we must consider them sufficiently different that we can study them in ways that are ethically objectionable for studying fellow humans."

Public Health Service (PHS) 1996. U.S. Government Principles for the Utilization and Care of Vertebrate Animals Used in Testing, Research, and Training. In Guide for the Care and Use of Laboratory Animals National Research Council 117-118. National Academy Press, Washington
Principle IV states that "Proper use of animals, including the avoidance or minimization of discomfort, distress, and pain when consistent with sound scientific practices, is imperative. Unless the contrary is established, investigators should consider that procedures that cause pain or distress in human beings may cause pain or distress in other animals."

Reese EP 1991. The role of husbandry in promoting the welfare of laboratory animals. In Animals in Biomedical Research Hendriksen CFM, Koeter HBWM (eds), 155-192. Elsevier, Amsterdam, NL
"That many scientists lack detailed information about their animals, especially their behavior, is distressing and reflects a serious disregard for the single most important element of their research. ... The animal is the key to the entire experiment. ... There is only one 'right' attitude, and that is respect for the individual animal."

Röder EL, Timmermans PJA 2002. Housing and care of monkeys and apes in laboratories: adaptations allowing essential species-specific behaviour. Laboratory Animals 36, 222-241
"An animal is not a survival machine but a genetically programmed organism. A machine 'survives' longest if it is maintained properly but not used. An animal, however, needs to use the functions that evolved for its survival, in order to keep those functions from decay and deterioration. Whoever deliberately chooses a species because of its specific properties, in his own interest should be expected to take care that these properties remain unimpaired."

Reinhardt V 1996. Letter to the Editor. Lab Animal 25(5), 42
"I was a bit surprised that the animals of my article lost their biological gender and were referred to in the neuter gender, like things. Perhaps this sounds more scientific, but it actually is scientifically incorrect. Animals with neuter gender cannot reproduce. A female is a 'she' and not an 'it', and a male is a 'he' and not an 'it'."

Schwindaman D 1991. The 1985 animal welfare act amendments. In Through the Looking Glass. Issues of Psychological Well-being in Captive Nonhuman Primates Novak MA, Petto AJ (eds), 26-32. American Psychological Association, Washington
"While we [veterinarians] pledge to take responsibility for the welfare of animals, we also vow to use scientific knowledge and skills for the advancement of medical knowledge. The wise composer of this oath saw no conflict between relieving animal suffering and advancing science. Indeed, there is none."

Spaeth GL 1994. Editorial: Caring for animals, caring for ourselves. Ophthalmic Surgery 25, 426
"Our behavior to other creatures reflects our own characters. We are shaped by what we do. When we act uncaringly toward experimental animals we become uncaring human beings. What is the worth of medical miracles achieved at the cost of inflicting trauma on others that cannot help but scar our own characters? When we act uncaringly towards experimental animals, we damage ourselves. When we hurt experimental animals, we hurt ourselves."

Traystman RJ 1987. ACUC, who needs it? The investigator's viewpoint. Laboratory Animal Science 37(Special issue), 108-110
"The investigator, above all, wants to pursue his or her research activities, be they of basic science or clinical nature. The academic and intellectual freedom to pursue these activities is crucial to the livelihood of any investigator... Most investigators think only briefly about the care and handling of their animals and clearly have not made it an important consideration in their work. .. All investigators consider themselves upstanding citizens of excellent ethical and moral character. Their feeling may be that since they are moral and ethical in every sense of the word, they are quite capable of monitoring their own animals without outside interference."

Zbinden G 1985. Ethical consideration in toxicology. Food and Chemical Toxicology 23, 137-138
"Toxicologists must realize that their important mission ... does not give them an unconditional license to kill as many animals as they wish and hide behind regulatory requirements, testing guidelines and bureaucratic prescriptions for good laboratory practice."

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