Short Communication: Using the Mesh Ceiling as a Food Puzzle to Encourage Foraging Behaviour in Caged Rhesus Macaques (Macaca Mulatta)

V. Reinhardt
Wisconsin Regional Primate Research Center, 1223 Capitol Court, Madison, WI 53715, USA




An attempt was made to encourage more foraging behaviour in eight pair-housed adult rhesus macaques (Macaca mulatta). No special device and no special food were used.

Daily commercial dry food rations (238g per animal) consisting of 33 bar-shaped or 16 star-shaped biscuits per animal were placed on the mesh ceiling of the cages instead of in the feed-boxes. This induced an 80-fold increase (17.0 vs 1362.9s) and 289-fold increase (12.3 vs 3551.4s), respectively, in foraging time. The animals spent on average 9.6 per cent and 24. 7 per cent respectively of four-hour observation sessions foraging for biscuits from the mesh ceiling. Working for their food did not discourage them from eating all left-overs in the course of a day regardless of the shape of the biscuits.

It was concluded that the new feeding procedure enhanced the animals' behavioural well-being by encouraging foraging activities thereby helping to counteract understimulation.

Keywordsanimal welfare, behavioural well-being, foraging, housing, rhesus macaques


© 1993 Universities Federation for Animal Welfare
Animal Welfare 1993, 2: 165-172
This article has been reproduced with permission of the publisher.



Chronic understimulation is a major problem for caged non-human primates. The situation is unsatisfactory for both the animal, which is deprived of expressing species-typical activities, and for the scientist who has to consider undefinable variables associated with possibly decreased well-being of the research subject. This issue has recently been taken into account by US federal rules which stipulate that the environment of such animals 'must be enriched by providing means of expressing noninjurious species-typical activities' (US Department of Agriculture 1991). Of these activities, foraging is predominant in wild and feral animals (eg Teas et al 1980, O'Keeffe & Lifshitz 1985, Malik 1986, Seth & Seth 1986, Malik & Southwick 1988, Marriott 1988). Caged animals, however, have little or no opportunity to express foraging activities because processed food is usually directly accessible. Environmental enrichment strategies have therefore largely focused on the development of devices that enhance more food retrieval behaviour under such unnatural conditions. The following devices have been described: pickup boards (Moazed & Wolff 1988, Evans et al 1989), puzzle feeders (Line & Houghton 1987, Bloom & Cook 1989, Line et al 1989, Murchison 1991, Gilloux et al 1992, Heath et al 1992, Murchison 1992), foraging boxes (Meunier et al 1989), food dispensers (Preilowski et al 1988, Markowitz & Line 1989, Gullekson et al 1991, Line & Morgan 1991), fleece boards (Bayne et al 1991), fleece cushions (Lam et al 1991), turf boards (Bayne et al 1992). Such foraging devices are relatively expensive and their maintenance work-intensive, requiring extra baiting with supplemental food items and regular cleaning and sanitation.

The present study is based on the premise that any foraging enhancement programme has to be inexpensive, both in terms of material and maintenance, to make it attractive to institutions with a large number of animals. Standard dry food rations were used to foster foraging activities in caged rhesus macaques. No special device was required, but commercial food biscuits were placed on the mesh ceilings of the cages instead of in the feed-boxes. This technique had originally been developed for group-housed rhesus macaques living in pens (Reinhardt 1992). It was hypothesized that total foraging time would be increased substantially, when the animals were obliged to retrieve the biscuits one by one using their manipulative skills.




The subjects of this study were eight adult (six years old), physically and behaviourally healthy (no clinical disease symptoms and no behavioural disorders) male rhesus macaques (Macaca mulatta). They shared a room with 101 conspecifics and were kept as four compatible pairs, each pair in a 70 x 150 x 77cm high lower-row cage, provided with a privacy panel, two diagonally suspended perches and two gnawing sticks. Room temperature was maintained at 20-22~C, with a relative air humidity of approximately 50 per cent and a 12h light/dark (0630h/1830h) cycle. A visual health check of every animal was done between 0645h and 0715h; this was followed by cage washing with pressurized water. Drop pans were flushed at two-hour intervals.

Each pair was fed a standard ration of 476g commercial dry food (15% crude protein) at 0900h, supplemented with fruit and bread or whole peanuts at 1600h. The food was normally placed in feed-boxes, each 14cm wide, 7cm deep, 17cm high, mounted 40cm off the cage floor over a 73 x 47mm access hole cut into the mesh on the front of each half of the cage. Water was available ad libitum. The dry food ration was offered in one of two different forms:

a. Thirty-two large biscuits (star-like shape with four spikes, about l5mm long and l5mm wide, protruding from a sphere measuring approximately 3Omm in diameter; Purina Monkey Chow No 5037) per pair.
b. Sixty-six small biscuits (bar-like shaped, about 4Omm long, 24mm wide and l6mm thick; Purina Monkey Chow No 5038) per pair.

    Each pair was subjected to the following experimental feeding protocol at 0900h:

    Day 1 (control situation A)
    The ration of small biscuits was equally distributed into the two feed-boxes.

    Days 2-14 (habituation A)
    The ration of small biscuits was distributed on the 22 x 22mm square mesh ceiling, instead of into the feed-boxes.

    Day 15 (control situation B)
    The ration of large biscuits was equally distributed into the two feed-boxes.

    Days 16-28 (habituation B)
    The ration of large biscuits was distributed on the square mesh ceiling, instead of into the feed-boxes.

    Time spent retrieving biscuits was recorded for each partner of each pair simultaneously during the two control situations, ie days 1 and 15, and at the end of the two habituation periods, ie days 14 and 28, from 0900h to 1300h. Retrieving was considered to be a foraging activity, ie the gathering of food (The Random House Dictionary of the English Language 1987). It included taking a biscuit out of the feed-box; manipulating a biscuit through the mesh of the ceiling (Figure 1); nibbling (biting at a biscuit that was partly protruding through the mesh, and pushing and pulling a biscuit or a fragment of it with the fingers and teeth through the mesh.

    Figure 1:Foraging for small biscuits placed on the mesh ceiling of the cage.

    Foraging activities did not include behaviours related to the actual consumption of food, eg emptying cheek pouches, chewing and swallowing.

    Recordings were carried out manually by the author who sat at a distance of approximately 2m from the centre of the cages.

    Biscuits that were thrown out of the feed-boxes or pushed over the edge of the ceiling of the cage were weighed and replaced. All animals were weighed at the beginning (day 1) and at the end (day 28) of the four-week study period.

    Statistical analysis was done using the Wilcoxon signed-rank test (Ferguson 1966).




    The eight rhesus macaques spent on average 17.0 and 12.3 seconds per four hours collecting their standard ration of small and large biscuits respectively from feed-boxes. Retrieving times were markedly longer when the same rations were placed on the mesh ceiling of the cages instead of in the feed-boxes (Table 1). Under these conditions, subjects spent on average 23.0 minutes, ie 9.6% of the four-hour test period retrieving small biscuits, and 59.2 minutes, ie 24.7% of the four hours retrieving large biscuits. The increase in retrieving time was significant for both types of biscuits (P<0.001; Table 1) with the amount of time devoted to the retrieval of large biscuits being significantly larger than that devoted to the retrieval of small biscuits (P<0.001; Table 1).

    Table 1 Time spent foraging by eight adult male rhesus macaques for commercial dry food presented in four different ways.

      Time spent foraging (s/4h)
    Paired partners Small biscuits Large biscuits
      In feed-box On ceiling In feed-box On ceiling




















    Per cent/4h





    When small or large biscuits were presented in the feed-boxes, individuals quickly took a few pieces in their cheek pouches and threw most of the remainder on to the floor of the cage while starting to eat. Feed-boxes were emptied within 7 to 28 minutes. When biscuits were placed on the mesh ceiling, retrieved pieces were never thrown on the floor but were either stored in the cheek pouches or eaten directly. Three pairs of macaques retrieved the last piece of their small biscuit ration during the second hour, the other pair during the fourth hour. No pair completely retrieved its large biscuit ration during the test period and subjects continued foraging on average 12.1 per cent of the time during the fourth hour. There were no left-overs by late afternoon, ie 1700h.

    Total food wastage (whole biscuits and fragments of biscuits thrown out of the feed-boxes or pushed over the edge of the ceiling of the cage) of all eight subjects was 0.3 per cent and 1.3 per cent when small and large biscuits respectively were placed in feed-boxes, 1.6 per cent and 2.1 per cent when small and large biscuits were distributed on the mesh ceiling.

    Mean body-weight balance of the eight rhesus macaques during the four-week study period was +2.5 per cent (day 1: 7.48 ± 0.88kg, day 28: 7.67 ± 0.76kg).




    The present data support the hypothesis that foraging activity can be enhanced substantially in adult rhesus macaques by simply placing the standard biscuit ration on the mesh ceiling of their cages instead of in the feed-boxes. The increase in foraging was determined by the size/configuration of the biscuits. Small, bar-shaped biscuits were relatively easy to manipulate, break and pull through the mesh; they induced an 80-fold extension of foraging time. Large, star-shaped biscuits were more difficult to pull through the mesh once all protruding parts were broken away; consequently more work was required to retrieve them and the increase in foraging time was even higher, ie 289-fold.

    Food wastage was minimal. It could probably have been avoided altogether by fixing rims around the top of the cages.

    The animals had to work for their food, but this did not discourage them from eating all left-overs in the course of a day regardless of the size of the biscuits. This ensured an adequate calorific intake, reflected in a moderate increase of the subjects' body-weight during the four-week study period.

    The present routine feeding technique stimulated adult rhesus macaques to spend on average 23 and 59 minutes to perform skillful food retrieval behaviours of small and large biscuits respectively. These activities cannot be claimed to be species-typical due to the artificial context, but they are foraging, ie food gathering behaviours in the true sense. Working for their food, rather than directly eating it, is likely to enhance the animals' behavioural well-being (O'Neill 1988, Bayne et al 1992).



    Animal welfare implications

    Distributing the standard food ration of caged rhesus macaques on the mesh ceiling of their cages instead of in feed-boxes resulted in a marked increase of foraging time which promoted the subjects' well-being by helping to counteract understimulation. Making the animals work for their food did not jeopardize their general health status as reflected in body-weight maintenance.




    I am grateful to Dan Houser, Chris Nywall and my wife Annie for critically reading this manuscript and to Jackie Kinney for proof reading it.

    Supported by USPHS, NIH grant RR-00167. Publication number 32-053 WRPRC.




    Bayne K, Mainzer H, Dexter S, Campbell G, Yamada F and Suomi 5 1991 The reduction of abnormal behavior in individually housed rhesus monkeys (Macaca mulatta) with a foraging/grooming board. American Journal of Primatology 23: 23-35

    Bayne K, Dexter S, Mainzer H, McCully C, Campbell G and Yamada F 1992 The use of artificial turf as a foraging substrate for individually housed rhesus monkeys (Macaca mulatta). Animal Welfare 1: 39-53

    Bloom K R and Cook M 1989 Environmental enrichment: behavioral responses of rhesus to puzzle feeders. Lab Animal 18(5): 25-31

    Evans H L, Taylor J D, Ernst J and Graefe J F 1989 Methods to evaluate the wellbeing of laboratory primates: comparisons of macaques and tamarins. Laboratory Animal Science 39: 318-323

    Ferguson G A 1966 Statistical Analysis in Psychology and Education. McGraw Hill: New York

    Gilloux I, Gurnell J and Shepherdson D 1992 An enrichment device for great apes. Animal Welfare 1: 279-289

    Gullekson R, Bench L, Harrigan K and Pyle K 1991 Seed-feeder as a foraging device for singly housed cynomolgus monkeys (Macaca fascicularis). Lab Animal 20(6): 44-46

    Heath S, Shimoji M, Tumanguil J and Crockett C 1992 Peanut puzzle solvers quickly demonstrate aptitude. Laboratory Primate Newsletter 31(1): 12-13

    Lam K, Rupniak N M J and Iversen S D 1991 Use of a grooming and foraging substrate to reduce stereotypies in macaques. Journal of Medical Primatology 20: 104-109

    Line S W and Houghton P 1987 Influence of an environmental enrichment device on general behavior and appetite in rhesus macaques. Laboratory Animal Science 37: 508 (Abstract)

    Line S W and Morgan K N 1991 The effects of two novel objects on the behavior of singly caged adult rhesus macaques. Laboratory Animal Science 41: 365-369

    Line S W, Markowitz H, Morgan K N and Strong S 1989 Evaluation of attempts to enrich the environment of single-caged nonhuman primates. In Driscoll J W (ed) Animal Care and Use in Behavioral Research: Regulations, Issues and Applications pp103-1 17. National Agricultural Library: Beltsville

    Malik 11986 Time budgets and activity patterns in free-ranging rhesus monkeys. In Else J G and Lee P C (eds) Primate Ecology and Conservation p105-1 14. Cambridge University Press: Cambridge

    Malik I and Southwick C 1988 Feeding behavior and activity patterns of rhesus monkeys (Macaca mulatta) at Tughlaqabad, India. In Fa J E and Soutliwick C (eds) Ecology and Behavior of Food-Enhanced Primate Groups pp95-111. Alan R Liss: New York

    Markowitz H and Line S 1989 Primate research models and environmental enrichment. In Segal E F (ed) Housing, Care and Psychological Well-Being of Captive and Laboratory Primates pp202-212. Noyes Publications: Park Ridge

    Marriott B M 1988 Time budgets of rhesus monkeys (Macaca mulatta) in a forest habitat in Nepal and on Cayo Santiago. In Fa J E and Southwick C (eds) Ecology and Behavior of Food-Enhanced Primate Groups pp125-149. Alan R Liss: New York

    Meunier L D, Duktig J T and Landi M 5 1989 Modification of stereotypic behavior in rhesus monkeys using videotapes, puzzlefeeders, and foraging boxes. Laboratory Animal Science 39: 479 (Abstract)

    Moazed T C and Wolff A V 1988 The raisin board as an environmental enrichment tool for laboratory primates. Laboratory Primate Newsletter 27(1)16

    Murchison M A 1991 PVC-pipe food puzzle for singly caged primates. Laboratory Primate Newsletter 30(3): 12-14

    Murchison M A 1992 Task-oriented feeding device for singly caged primates. Laboratory Primate Newsletter 31(1): 9-11

    O'Keeffe R T and Lifshitz K 1985 A behavioral profile for stumptail macaques (Macaca arctoides). Primates 26: 143-160

    O'Neill P 1988 Developing effective social and environmental enrichment strategies for macaques in captive groups. Lab Animal 17(4): 23-36

    Preilowski B, Reger M and Engele H 1988 Combining scientific experimentation with conventional housing: a pilot study with rhesus monkeys. American Journal of Primatology 14: 223-234

    Reinhardt V 1992 Foraging for commercial chow. Laboratory Primate Newsletter 31(2): 10

    Seth P K and Seth S 1986 Ecology and behaviour of rhesus monkeys in India. In Else J G and Lee P C (eds) Primate Ecology and Conservation pp89-103. Cambridge University Press: Cambridge

    Teas H, Richie T, Taylor H and Southwick C 1980 Population patterns and behavioral ecology of rhesus monkeys (Macaca mulatta) in Nepal. In Lindburg D G (ed) The Macaques: Studies in Ecology, Behavior and Evolution pp247-262. Van Nostrand Reinhold: New York

    The Random House Dictionary of the English Language, 2nd Edition 1987 Random House: New York

    US Department of Agriculture 1991 Animal Welfare, Standards, Final Rule. Federal Register 56: 6426-6505

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    Animal Welfare 1993, 2: 165-172
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