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American Journal of Primatology 23:23-35 (1991) The Reduction of Abnormal Behaviors in Individually Housed Rhesus Monkeys (Macaca mulatta) With a Foraging/Grooming Board K. BAYNE, H. MAINZER, S. DEXTER, G. CAMPBELL, F. YAMADA, AND S. SUOMI Office of Animal Care and Use, Office of the Director (K.B., H.M., S.D.), Laboratory of Statistical and Mathematical Methodology, Division of Computer Research and Technology (G.C., F.Y.), and Laboratory of Comparative Ethology, National Institute of Child Health and Human Development (S.S.), National Institutes of Health, Bethesda, Maryland A new environmental enrichment device, termed a “foraginglgrooming board,” was presented to 8 individually housed rhesus monkeys for the explicit purpose of reducing the level of aberrant behaviors manifested by these animals. The device, consisting of a piece of plexiglass covered with artificial fleece, had particles of food treats rubbed into it and was at- tached to the outside of each animal’s home cage. All animals foraged from the board to the point that a significant reduction in the level of abnormal behavior was noted. Most animals also groomed the fleece covering the board, utilizing the same motor patterns that would be directed toward grooming another monkey. These boards are inexpensive to construct and easy to sanitize, and do not require placing animal facility personnel at risk to maintain them. Key words: environmental enrichment, fleece, aberrant behavior INTRODUCTION The occurrence of abnormal behaviors in individually housed nonhuman pri- mate populations is well documented [Harlow and Harlow, 1962; Berkson, 1967; Erwin & Deni, 1979; Goosen, 19811. Proposed methods of reducing or eliminating these aberrant behaviors have been varied [Reinhardt et al., 1987a,b; Line et al., 1989; Wolff, 19891,with two main approaches typically being taken for behavioral modification. The first approach encourages the replacement of abnormal behav- iors with behaviors considered normal for the species (e.g., substituting social behavior for self-abuse by providing a cage companion).The second approach elicits novel behaviors from the animal (working for a food reward by operant techniques, participation in computer games, etc.) which occupy time in the behavioral reper- toire, thereby reducing the time available for the occurrence of undesirable behav- iors. An increasingly pressing need to devise environmental strategies for captive nonhuman primates, stimulated by the passage of the 1985 amendment to the Received for publication April 2, 1990; revision accepted August 27, 1990. Address reprint requests to Dr. K. Bayne, Bldg. 14DIRm. 313, National Institutes of Health, 9000 Rockville Pike, Bethesda, MD 20892. 0 1991 Wiley-Liss, Inc.

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American Journal of Primatology 23:23-35 (1991)

The Reduction of Abnormal Behaviors in Individually Housed Rhesus Monkeys (Macaca mulatta) With a Foragi ng/G rooming Board

K. BAYNE, H. MAINZER, S. DEXTER, G. CAMPBELL, F. YAMADA, AND S. SUOMI Office of Animal Care and Use, Office of the Director (K.B., H.M., S.D.), Laboratory of Statistical and Mathematical Methodology, Division of Computer Research and Technology (G.C., F.Y.), and Laboratory of Comparative Ethology, National Institute of Child Health and Human Development (S.S.), National Institutes of Health, Bethesda, Maryland

A new environmental enrichment device, termed a “foraginglgrooming board,” was presented to 8 individually housed rhesus monkeys for the explicit purpose of reducing the level of aberrant behaviors manifested by these animals. The device, consisting of a piece of plexiglass covered with artificial fleece, had particles of food treats rubbed into it and was at- tached to the outside of each animal’s home cage. All animals foraged from the board to the point that a significant reduction in the level of abnormal behavior was noted. Most animals also groomed the fleece covering the board, utilizing the same motor patterns that would be directed toward grooming another monkey. These boards are inexpensive to construct and easy to sanitize, and do not require placing animal facility personnel at risk to maintain them.

Key words: environmental enrichment, fleece, aberrant behavior

INTRODUCTION The occurrence of abnormal behaviors in individually housed nonhuman pri-

mate populations is well documented [Harlow and Harlow, 1962; Berkson, 1967; Erwin & Deni, 1979; Goosen, 19811. Proposed methods of reducing or eliminating these aberrant behaviors have been varied [Reinhardt et al., 1987a,b; Line et al., 1989; Wolff, 19891, with two main approaches typically being taken for behavioral modification. The first approach encourages the replacement of abnormal behav- iors with behaviors considered normal for the species (e.g., substituting social behavior for self-abuse by providing a cage companion). The second approach elicits novel behaviors from the animal (working for a food reward by operant techniques, participation in computer games, etc.) which occupy time in the behavioral reper- toire, thereby reducing the time available for the occurrence of undesirable behav- iors.

An increasingly pressing need to devise environmental strategies for captive nonhuman primates, stimulated by the passage of the 1985 amendment to the

Received for publication April 2, 1990; revision accepted August 27, 1990.

Address reprint requests to Dr. K. Bayne, Bldg. 14DIRm. 313, National Institutes of Health, 9000 Rockville Pike, Bethesda, MD 20892.

0 1991 Wiley-Liss, Inc.

24 I Bayne et al.

Animal Welfare Act, prompted our examination of foraging as a means of reduc- ing abnormal behaviors in singly housed rhesus monkeys (Macaca mulatta). In the natural setting, foraging behaviors of nonhuman primates occupy from 7% to 65% of the diurnal activity budget [Milton, 1980; Herbers, 1981; Strier, 1987; Malik & Southwick, 1988; Marriott, 1988; O’Neill et al., 19891. In some free-ranging rhesus monkey populations, foraging has been described as the “single most time-con- suming behavior” during some seasons of the year [Malik & Southwick, 19881. In laboratory settings, devices that increase the amount of time nonhuman primates spend foraging have been shown to have beneficial effects on the animals [Ander- son & Chamove, 1984; McGrew et al., 19861.

As Novak et al. [in press1 have discussed, laboratory environments can be made more naturalistic by modelling activities and behaviors in which free- ranging animals engage. This approach mimics natural situations by paralleling function rather than structure. Foraging behaviors can be quite time-consuming and appear to be instinctual, as defined by James [19611. Several investigators have either hypothesized or actually demonstrated [Rosenblum & Smiley, 1984; Line & Houghton, 19871 that this behavior pattern would be relatively easy to encourage in individually housed macaques. In such studies, foraging behaviors serve to replace undesirable abnormal behaviors occurring in these animals.

Foraging behaviors among free-ranging animals include search patterns and consumptive processes for fruit, insects, nectar, leaves, and even dirt [Clutton- Brock, 1977; Garber, 1987; Oates, 1987; Marriott, 19881. The goal of increasing the amount of time spent on food processing and consumption by nonhuman primates in the laboratory can be achieved by 1) hiding the food and requiring the animal to search for it [Anderson & Chamove, 1984; Boccia, 1989al; 2) requiring the animal to solve a puzzle or task to gain access to the food [Rosenblum & Smiley, 1984; Line & Houghton, 1987; Gust et al., 1988; Bloom & Cook, 1989; Maki et al., in press]; or 3) giving the food whole to the animal to increase time spent on processing the food to reach the edible parts [Bloomsmith & Maple, 19881. Al- though some species spend more time engaged in food consumption when the food is presented whole [Lindburg & Smith, 19881, it was hypothesized that reduction of the food size presented to the rhesus monkey might also serve to extend the time spent in foraginglfeeding behaviors.

METHODS Subjects

Eight adult rhesus monkeys (2 males and 6 females) served as subjects. All had been individually housed for over 1 year in the same animal holding room. They ranged in weight from 4-10 kg at the start of the study. Table I provides back- ground information on the subjects, including age, sex, rearing history, and gen- eral description of each animal’s characteristic pattern of abnormal behavior, or abnormal “behavioral fingerprint.”

Description of Apparatus The opportunity to forage was provided by means of a “foraging/grooming

board” which was attached to the outside of the cage (thereby reducing safety risks to the animal care staff). The board, developed in our laboratory, was a .1 m2 piece of plexiglass 12 mm in thickness. A pair of 9 mm holes was drilled through two opposing sides of the plexiglass for the purpose of attaching a U-bolt to the board. A double-ended snaphook attached to the U-bolt secured the board to the case side or front. Before fitting the hardware to the board, the plexiglass was covered with nontoxic, white artificial shearling or fleece (obtained from a fabric store) which

ForaginglGrooming Board for Primates I 25

TABLE I. Background Information on Subjects

Animal Age no. Sex (yrs) Rearing history" Informal observations of the behavioral profile

AA13

AE53

AH57

H41

554

Q96

V63

W86

F

F

M

F

F

M

F

F

14 Nursery/peer-reared

12 Partial isolate

10 Nursery/peer-reared

23 Motheripeer-reared

21 Partial isolate

18 Motherlpeer-reared

16 Nurserylpeer-reared

15 Mothedpeer-reared

Trance-like stare; sits at a tilt, rubs finger along roof of mouth and regurgitates into the cheek pouches; sucks big toe; circles quite frequently; fairly aggressive

Circles a t a trot; hyperactive; very alert; plucked hair on right cheek; occasionally observed to eat feces and drink urine

Repeatedly stands up facing left wall and rocks back and forth briefly, then drops down onto elbows. While down on forearms, pokes left middle finger in mouth repeatedly. Resumes sitting position with cheek pouches full of regurgitation; circles; masturbates

Quite inactive; circles occasionally; masturbates. Began to self-clutch her dorsum with both hands

Sucks big toe, self-clasps entire body and head; sleeps with big toe in mouth; some circling, bouncing; salutes; not very attentive to environment

Fairly inactive; circles periodically; drinks water regularly; occasionally masturbates

Leans to side, strums bars of cage, dips head and regurgitates saliva; circles; threatens monkeys across the way consistently; occasional head toss while circling

occasionally observed drinking urine and eating feces

Fairly inactive; alert; some slow circling;

Wsing Mason, W.P. (1968) definitions of rearing conditions

had been tailored for this purpose (see Fig. 1). Fleece attached to the case in this manner could not be torn off by the animal. This use of the fleece represents a novel manner of presenting this substrate to the rhesus monkey subjects. Figure 2 shows the assembled foraging board being used by a monkey. Flavored particles of food (purchased from Bioserve, Inc.) were rubbed into the fleece prior to attaching the device to the cage. Flavors used during the course of the study included ba- nana, cherry, strawberry, and orange. The entire surface of the board was covered with the food on a daily basis. Some spillage was incurred when the board was positioned vertically against the cage.

Throughout the experimental period the fleece was routinely machine washed in hypochlorite bleach and laundry detergent once a week. The fleece was dis- carded and replaced approximately once every 3 months. If the fleece became unusually soiled before the regular washing schedule, it was replaced at that time. The plexiglass board and hardware stayed attached to the cage through the cage- washer for sanitization.

Experimental Design and Data Collection An A-B-A paradigm was used to assess behavioral effects of exposure to the

foraging device. Pre-experimental (PRE) behavioral data were collected on the

26 I Bayne et al.

artificial shearling (fleece)

U-bolt

. double-ended snap hook

Fig. 1. Schematic of foragingigrooming board, rear view.

animals for approximately 1 month to quantify the frequency and duration of aberrant behaviors present in each subject and to qualify these abnormal behav- iors. Each animal was observed for four 30 minute sessions during this phase, for a total of 16 hours overall.

Each animal was then monitored with the experimental device continuously attached to its cage for a minimum of 6 months. These observation sessions were also of 30 minute duration. During this phase (EXP) each animal was scored 20 times, for a total of 80 hours overall.

To determine if any lingering behavioral effects occurred from the presence of the device and the opportunity to engage in naturalistic behaviors, the foraging1 grooming boards were removed for 1 month and home-cage behaviors without the boards present were recorded for an additional month (POST). As in the PRE condition, four 30 minute sessions were collected for each animal in the POST phase.

A barcode recording system [Line, 19871 was used in conjunction with a lap-top Tandy 102 computer and an IBM-XT to record the frequency and duration of predetermined behavioral categories during 30 minute observation sessions. Op- erational definitions of these categories are provided in Table 11. The observer sat quietly approximately 1 m from the subject, directly in front of the animal’s cage. At all times the observer took care to avoid eye contact with the subject. The animals were habituated to the presence of the observer for 1 week prior to initi- ation of the study. In contrast to the evaluation of the impact of the presence of an observer done in other studies [Kalin & Shelton, 19891, our experience has been that rhesus monkey subjects readily adapt to the presence of an observer [Line, 1987; Bayne et al., submitted], to the point where it is not uncommon for animals to fall asleep while a familiar observer is in the room.

STATISTICAL ANALYSIS For purposes of analysis, the wide variety of abnormal behaviors recorded were

collapsed into four general categories: excessive locomotion, stereotypic, self-di- rected, and cage-directed (see Table 11). An overall analysis and a pair-wise anal- ysis of the differences among the three conditions (PRE, EXP, POST) were applied to the data. Additionally, Page’s test [Hollander & Wolf, 19721 was used to eval- uate the data for changes over time in the EXP phase. Appendix A presents a detailed explanation of these analyses.

RESULTS All animals displayed a minimum of four different types of abnormal behav-

iors during the baseline sessions, which did not necessarily include behaviors from

ForaginglGrooming Board for Primates i 27

Fig. 2. Rhesus monkey V63 foraging from board, front view.

all categories of abnormal behavior. For the sum of these four, the mean durations and frequencies are presented for each monkey and overall in Tables I11 and IV. Also included are totals of the four types of behavioral pathology and self-grooming for all conditions, and the foraginglgrooming for the EXP condition.

The overall analysis of the four abnormal behaviors demonstrated that there was a significant difference among the three conditions for both duration (P < 0.0001) and frequency (P < 0.001) and that the EXP duration and frequency were significantly lower than PRE (P < 0.03, P = 0.002) and POST (P < 0.0001, P < 0.001) with no evidence for a difference between PRE and POST. The four abnor- mal categories were then examined separately. Locomotion occurred significantly less in the EXP condition than in the PRE duration (P = 0.02) and POST fre- quency (P = 0.03) conditions. It should be noted that self-directed behavior oc- curred at higher levels of duration and frequency in the POST condition than in the EXP phase (P < 0.0001, P < 0.0001). A significantly lower duration and frequency of cage-directed behavior was found in the EXP condition when com- pared with both PRE (P = 0.004, P < 0.002) and POST (P < 0.001, P < 0.002) conditions, respectively. No significant differences were noted for the miscella- neous stereotypic behavior category. Self-grooming duration was significantly re- duced in the EXP phase as compared with the PRE (P < 0.0002) and POST (P < 0.0005) conditions.

All subjects used the foraginglgrooming board immediately upon its presen- tation even though they had not been previously exposed to the food on the board. The mean percent of the time per session spent foraginglgrooming from the board was 40.4 (range = 17-59%). Figure 3 presents the average time spent foraging1 grooming for the 20 sessions over the 6 month EXP period for the abnormal be-

28 I Bayne et al.

TABLE 11. Behaviors Considered Abnormal

Excessive locomotion Circling Pacing Bouncing Somersaulting Rocking Spinning

Stereotypic The combination of idiosyncratic patterns of movements and postures which the animal manifests in a repetitive, seemingly non-goal oriented manner

Self-directed Self-abusive (self-biting and head-banging) Auto-erotic Suck Pluck hair (this behavior was considered abnormal when it created a bald area on the animal’s body or when the animal gave a distress vocalization, indicative of pain, concurrent with the plucking) Coprophagia Drink urine (note: urine dip-stick test was performed on subjects exhibiting this behavior to ensure that glucosuria was not the cause of urine drinking) Excessive grooming Le., to the point of making a bald area on the body) Posturing (e.g., saluting, self-clasping)

Cage-directed Excessive cage manipulation (i.e., animal could only be distracted from this activity for short periods of time) Cage biting

(Reproduced from Erwin & Deni, 1979, with permission of the publisher.)

haviors and for the groominglforaging with the board. The nonparametric test of Page rejected the hypothesis of no time trend in favor of the alternatives that the abnormal behaviors declined over time (P < 0.001) and the time with the fleece increased (P < 0.0001). Individual preferences for flavors were readily apparent. The order of flavor preference for these animals was orange, banana, cherry, and strawberry.

Two predominant methods were used by the monkeys to forage: 1) the mon- keys would pick out individual particles with the thumb and forefinger, or 2) the monkeys would lick food particles directly off the fleece, with one modification of this being licking the hands and rubbing them on the fleece and then licking the food off the hands. Some of the subjects seemed to incorporate the foraginglgroom- ing board into their territory, as evidenced by the threat gestures they made at the experimenter only when the board was being detached from the cage.

A corollary behavioral benefit that was observed in the subjects was the use of the board for “social” grooming (i.e., a monkey grooming the fleece using the same actions it would direct toward another animal). One subject (V63) consistently assumed a posture that resembled an invitation to groom (arms extended upward, head tilted back, and chest thrust slightly outward) directed at the board similar to that described by Altmann [1962]. Many subjects continued to pick at the fleece long after the particles of food were gone, parting the fibers of the fleece to gain access to matter too small for the human observers to detect.

ForagingIGrooming Board for Primates I 29

TABLE 111. Mean Duration (SecondsV30 Minute Session of Recorded Behavior for Each Observation Condition

Total abnormal Animal no. Self- Cage- behaviors Self- Foraging/ condition Locomotion Stereotypic directed directed (with SD) groom grooming

AA13 PRE 184 EXP 132 POST 94

PRE 659 EXP 788 POST 661

PRE 84 EXP 57 POST 182

PRE 211 EXP 16 POST 12

PRE 16 EXP 14 POST 46

PRE 334 EXP 315 POST 117

PRE 632 EXP 86 POST 131

PRE 74 EXP 131 POST 20

AE53

AH57

H4 1

554

Q96

V63

W86

Total mean duration overall subjects

PRE 274 EXP 192

12 45 31

6 2 0

72 9 0

16 3 0

31 88 16

0 0 0

2 135 76

67 15 0

26 37

POST 158 15

174 26

770

4 36 77

0 25 12

5 51

475

322 256

1,416

14 14

226

187 54

288

26 107 72

91 71

417

114 28 9

10 2 3

12 4

12

9 20 1

49 15 19

72 4

373

14 32 77

76 22

5

44 16 62

484 (408) 231 (203) 904 (636)

678 (316) 828 (455) 741 (298)

168 (68) 95 (135) 206 (87)

241 (231) 90 (96)

488 (116)

418 (410) 374 (368)

1,496 (398)

421 (616) 333 (340) 716 (365)

834 (706) 306 (353) 572 (240)

243 (134) 274 (365) 97 (85)

436 316 653

33 32

136

150 110 136

248 54

251

292 392 166

379 141 96

20 38

271

328 15

266

191 92

449

205 109 221

863

305

608

569

943

870

1,056

601

727

Only one subject, AE53, exhibited little interest in the board initially. This animal's predominant behavior was trotting around the cage, and during most observation sessions, she only broke from this stereotypy for very short periods of time. At the start of the study AE53 was thin and had a rough hair coat. However, this animal's physical condition improved during the course of the study as she began to sit for longer periods of time in front of the board to foragelgroom, in contrast to her initial pattern of grabbing at the food particles on the board while quickly circling past.

30 I Bayne et al.

TABLE IV. Mean Frequency130 Minute Session of Recorded Behavior for Each Observation Condition

~

Total abnormal Animal no. Self- Cage- behaviors Self- Foraging1 condition Locomotion Stereotypic directed directed (with SD) groom grooming

AA13 PRE 13.0 EXP 9.9 POST 5.0

PRE 22.0 EXP 25.0 POST 33.0

PRE 3.8 EXP 5.1 POST 15.3

PRE 12.3 EXP 2.2 POST 2.0

PRE 1.3 EXP 0.9 POST 2.5

PRE 4.3 EXP 6.2 POST 4.8

PRE 17.8 EXP 3.5 POST 8.0

PRE 4.5 EXP 6.2 POST 3.8

AE53

AH57

H41

554

Q96

V63

W86

Total mean frequency overall subjects

PRE 9.8 EXP 7.4

1.0 1.5 1.5

0.8 0.2 0

6.8 1.2 0

1.5 0.2 0

0.3 3.9 1.8

0 0 0

0.5 2.3 2.5

2.8 1.1 0

1.7 1.3

POST 9.3 0.7

0.5 0.8 1.8

0.3 1.9

16.3

0 0.6 1 .o

0.3 0.8 5.8

6.8 2.6

15.8

0.5 0.7 1.3

6.0 0.4 5.3

1.5 3.2 3.0

2.0 1.3 6.3

4.8 2.4 1.0

1.0 0.2 0.8

1.3 0.7 2.0

1.0 0.9 0.3

1.5 1.3 2.8

2.5 0.7 1.5

1.5 1.1 3.5

9.8 1.0 0.8

2.9 1.0 1.6

19.3 (6.7) 14.5 (17.1) 9.3 (5.8)

24.0 (8.2) 27.3 (16.2) 50.0 (24.8)

11.8 (5.6) 7.5 (8.0)

18.3 (6.1)

15.0 (11.1) 4.0 (7.3) 8.0 (2.2)

9.8 (8.8) 8.6 (5.2)

22.8 (12.3)

7.3 (6.7) 7.5 (4.6) 7.5 (7.4)

25.8 (20.5) 7.3 (4.6)

19.3 (9.0)

18.5 (13.0) 11.4 (9.4) 7.5 (5.8)

16.4 11.0 17.8

1.3 1.3 2.0

4.0 2.0 2.5

4.5 1.1 6.0

4.5 2.2 3.5

2.5 3.4 3.8

1.5 1.8 4.0

3.3 0.6 4.5

3.5 1.6 6.3

3.1 1.8 4.1

7.4

6.0

5.7

4.2

8.9

6.7

12.8

6.9

7.3

A record of the body weights of the subjects was kept to determine if the provision of nutritionally balanced food particles in addition to the routine twice daily feeding regimen resulted in an unusual weight gain. On the average, the monkeys gained only a little over 0.5 kg by the end of the study.

DISCUSSION Since the term “psychological well-being” (1985 amendment to the Animal

Welfare Act) did not originate from the scientific community and to date cannot be

ForagingIGrooming Board for Primates I 31

T 1400 3

0 5 10 1 5 20

SESSION I, - OCCURREWE OF ABNORMAL BEHAVIORS - USE OF FORAGINaMROOY(NQ BOARD

Fig. 3. board.

Comparison of trends in mean GEM) occurrence of abnormal behavior with use of foraging/grooming

easily defined by experts in primate behavior and biology, the approach taken in this study to improve animal holding conditions was by means of environmental enrichment. The ultimate goal of an enrichment technique should be a behavioral andlor physiological benefit. In this particular case, the provision of a foraging1 grooming board to individually housed rhesus monkeys resulted in an increase in normal behavior and a reduction in duration of abnormal behavior. Moreover, the mean time the animals spent foraginglgrooming continued to increase over the experimental sessions, rather than decline with time.

The participation by some animals in grooming activities directed at the board was also considered a positive response. Grooming is usually considered to be a tension-reducing component of the behavioral repertoire [Boccia, 1989b,c] and has been found to occupy approximately 15% of a rhesus monkey’s time [O’Neill et al., 19891; thus it is hypothesized that an animal grooming the fleece will be in a calmer mental state. The reduction in self-grooming was in all likelihood due to a shift in grooming activities towards the enrichment device. The reluctance with which some animals gave up their boards, as evidenced by facial and postural signals displayed when the boards were removed for cleaning, further supports the notion that these boards were attractive to the monkeys.

Although Novak et al. [in press1 caution that use of “analogous transposition” may fail when attempting to make the laboratory environment more naturalistic, mimicking the foraginglgrooming activities in which free-ranging macaques en-

32 I Bayne et al.

gage appears to be quite feasible. Indeed, all of the present subjects made use of the foraging/grooming board within the range of occurrence reported for natural pop- ulations of rhesus monkeys. No observable pattern of differences in board-use and behavioral modification could be identified relative to the animals’ rearing histo- ries.

In addition, anecdotal observations suggested that the manifestation of forag- ing behaviors appeared to be quite sensitive to the animal’s state of health and to changes in the animal’s environment. Specifically, AH57 stopped foraging for 2 days during the course of the study after he developed an infection in his leg. Also, four animals ceased foraging for 1 day when infant monkeys were moved into their holding room. These four subjects appeared to have a greater level of arousal than was typical of other monkeys in the room and they wers extremely attentive to their surroundings to the point where they could not be distracted by the presence of food.

It should be noted that a complete elimination of all abnormal behaviors for all animals was not achieved. However, a reduction in overall behavioral pathology was achieved to some degree for all animals probably due to replacement of the behaviors with foraginglgrooming. The decrease in self-directed and cage-directed behaviors seems a natural result of refocusing this attention on the grooming/ foraging board. Furthermore, only one animal, AE53, seemed resistant to increas- ing her foraginglgrooming time and reducing her time spent in stereotypic circling in the presence of the board. Berkson & Mason [19641 have reported that human patients who exhibit a high degree of stereotyped behavior are less susceptible to changes in “situational or stimulus” conditions. In addition, it has been docu- mented [Davenport & Berkson, 1963; Berkson & Mason, 19641 that human pa- tients manifesting a high level of stereotypy manipulate objects in the environ- ment less often than low level stereotypic patients.

One problem which must be addressed consistently for any enrichment device is the decline in usage and return to aberrant behaviors which can occur as the animal habituates to the presence of the device. No evidence of habituation was noted for the animals’ responsiveness to the foraginglgrooming board. In fact, as Figure 3 shows, use of the board actually increased with time. A similar finding has been reported for cynomolgus monkeys provided with foraging opportunity [Bryant et al., 19881. Although there are not enough data to draw absolute con- clusions, there is some indication that the removal of the enrichment device, with- out the substitution of another device, results in an increase in the performance of some abnormal behaviors. This trend is evidenced by the rise in duration of self- directed behavior. This finding should be considered when making programmatic decisions.

CONCLUSIONS

1. This technique elicited two normal behaviors from laboratory nonhuman primates: foraging and grooming.

2. A reduction in overall abnormal behavior was achieved while the grooming/ foraging board was present, although the animals returned to pre-experimental levels by 1 month after its removal.

3. The board was constructed at a low price (approximately $15 for materials) and was easy to sanitize.

4. From a husbandry perspective, it was especially important that animal facility personnel did not have to open the cage to maintain the device, thereby minimizing exposure to scratch or bite wounds.

ForagingIGrooming Board for Primates I 33

ACKNOWLEDGMENTS

Branson of the Medical Arts and Photography Program, NIH. The authors would like to recognize the photographic work of Mr. William

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LABORATORY PRIMATE NEWSLET-

APPENDIX A The statistic used for the overall analysis of differences among the three con-

ditions (PRE, EXP, POST) is based on a nonparametric test for ordered alterna- tives for the randomized block design, first introduced by Jonckheere [Hollander & Wolfe, 19721. The alternatives of interest to the null hypothesis of no difference among the three conditions are that for the sum of durations for the four abnormal categories, the ordering is EXPrPRErPOST or EXPsPOSTsPRE for the means, with at least one strict inequality for each order. (The foraginglgrooming board is of interest only if it reduces behavioral pathology.) The test statistic of Jonckheere for the analysis of a one-way layout for ordered alternatives is calculated for each monkey separately; these statistics are summed over monkeys [Jonckheere, 19541.

With two ordered alternatives, each is tested but the nominal P- values are doubled by the Bonferroni adjustment. If there is evidence to support either alter- native, a step-wise multiple comparison procedure is employed to investigate which pairs of conditions differ significantly. The theory of step-wise comparisons allows one to compare the three pair-wise alternatives a t the same level as the

ForagingIGrooming Board for Primates I 35

omnibus test [Campbell & Skillings, 19851. Here, the three pair-wise alternatives are EXPCPRE, EXP<POST, and PRE +POST. It is important to note that because the sample sizes in the three groups are different (4, 20, 41, it is more difficult to detect the third (pair-wise) alternative than the other two. The test statistic for the pair-wise analyses is the Mann-Whitney (or two sample Wilcoxon) test statistic for each monkey, summed over the monkeys. Only if there is evidence to support the contention that there are overall differences in the sum of the abnormal behaviors (frequency or duration) are the individual behaviors examined separately (loco- motion, stereotypic, self-directed, and cage-directed), in which case the process is repeated with each behavior.

Page’s test for ordered alternatives is used to examine the hypothesis of no change over time during the EXP phase for the two variables, total time engaged in abnormal behaviors, and total time spent in normative behaviors a t the forag- inglgrooming board. The alternative employed is a monotone one; namely, that over time the effect either is monotonically increasing or monotonically decreasing corresponding to increased interest or habituation.