Individual behaviour and activity rhythms of captive slow lorises (Nycticebus coucang)

Anim. Behav..

1969, 17, 664-669

INDIVIDUAL BEHAVIOUR AND ACTIVi~fY RHYTHMS O F CAPTIVE SLOW LORISES (NYCTICEBUS COUCANG) BY R I C H A R D T E N A Z A

Department of Zoology, University of California, Davis, California 95616 BRUCE A. ROSS & P R A Y O T T A N T I C H A R O E N Y O S

Medical Research Laboratory, SEATO Medical Research Project, Rajvithi Road, Bangkok, Thailand & G E R S H O N BERKSON

Delta Regional Primate Research Center light bulb installed on the back wall (Plate XV, Fig. 1C). The cages were placed side-by-side and stacked two high (Plate XV, Fig. 1B). Heavy brown wrapping-paper covering all but the front wall of each cage prevented visual contact between individuals. The cages were bare except for one or two plastic food bowls in each. The room in which the lorises were kept was walled with wire screening covered with clear plastic sheeting, so that the animals were exposed to the natural cycle of daylight and darkness in Bangkok. The animal house was cooler and quieter at night than it was during the day. The animals were fed on powdered-milk solution and whole fresh bananas during the study, and had been on a similar diet during most of their captive lives. Quantitative data were recorded on behaviour checklists which included the categories of activities noted in Table I. During the period of 22 to 3l August 1967, a total of 72 hr of tallying was compiled, 3 hr of recording being done for each hr in the day. Tallies were made at the rate of one every 5 min for each animal, i.e. twelve observations per animal per hr. During the observation periods an interval timer was set to ring every 5 min to signal the recording times. Sleeping animals were not aroused by the bell, but animals that were awake would occasionally turn toward the sound. To make an observation for tally purposes, the investigator glanced at an animal only long enough to determine what activity it was engaged in at that moment, usually a period of 2 or 3 sec. Then he recorded the observation on that individual's checklist, and went on to the next subject. Interrater agreement averaged 72 per cent. During preliminary observations, it was found that the lorises were less often disturbed by an observer behind a curtain than by one in

In their review of primate classification, Washburn & Hamburg (1965) noted the small number of studies on the behaviour of prosimians and called for an increased attention to this gi:oup in order to clarify its role in the evolution of the primates. Among the prosimians, detailed study of the Lorisinae has been limited to one study of Loris tardigradus, the slender lofts (Subramoniam 1957), although there has been considerable observation of a casual or restricted nature (Crandall 1964; Elliot & Elliot 1967; Hediger 1950; Hill 1953; Ilse 1955; MacKenzie 1929; Pournelle 1955; Sanderson 1957). One particular interest in this group is the analysis of their slow movements, the physiology of which is still quite obscure. In addition, the character of the social behaviour of these animals is still in question. For instance, although the slender loris is generally regarded as aggressive and difficult to keep with its own kind, Subramoniam (1957) showed that this is not necessarily the case. Furthermore, while it seems that in the forest slow lorises are ordinarily found alone (Elliot & Elliot 1967), in captivity they do well together and are believed to be sociable (Crandall 1964). The study reported here was intended to outline the major activities found in individual slow lorises and to describe their diurnal cycle in a laboratory situation in order to furnish a background for further laboratory studies. Method The subjects, three adult males and three adult females, were wild-caught animals captured in Thailand and housed in the SEATO Medical Research Laboratory, Bangkok, Thailand. None had been in captivity for less than 3 months. They were kept one to a cage in steel-framed 16-mm mesh wire cages. On the inside, each cage measured 71 cm back to front, 61 cm across, 53 cm from top to bottom and had a 5-W red 664

TENAZA et al. : BEHAViOUR AND ACTIVITY RHYTHMS OF SLOW LOR|SES

665

Table I. Number of Times Particular Behaviours Were Observed for Individuals and Their Sums Individual animals Activity category

1F

2F

3F

4M

All six animals 5M

6M

Sum

%

50

Locomotion Walking

23

70

40

128

82

105

448

Walking accompanied by perineal rubbing

11

18

8

5

31

25

98

Climbing

32

66

62

124

103

68

445

50

Sitting with head below level of shoulders

382

407

265

143

395

407

1999

78

Lying down

133

0

127

236

52

12

560

22

207

144

234

86

91

187

949

62

Sitting with hands on cage wall

14

25

t9

9

12

6

85

6

Standing erect on all fours

17

17

22

48

10

22

136

9

2

9

7

14

14

4

50

3

25

103

63

40

72

14

317

21

Scratching with hind foot

10

18

11

1

2

7

49

11

Licking body

96

75

72

25

61

84

413

89

Dip hand, then lick liquid from hand

0

0

18

1

0

0

19

21

Lap with muzzle in bowl

6

9

11

12

11

21

70

79

Ingestion of solid food (banana) Hold banana off floor with one or both hands

0

1

2

3

0

0

6

46

One or both hands placed on banana without lifting it from floor

1

0

0

0

1

0

2

15

Mouth contact only

1

0

0

0

1

3

5

39

Sleeping posture

Non-sleeping, non-locomotory Sitting, rear lowered, anterior elevated, hands and feet on cage floor

Crouched on all fours Standing upright with hands on cage wall Self-grooming

Ingestion of liquid (milk)

p l a i n view. Therefore, tallying was done from b e h i n d a black c u r t a i n 2.4 m wide by 1.2 m high, with peep holes, placed directly in front of the cages (Plate XV, Fig. 1A). Initially the c u r t a i n was placed 1.2 m from the cages, b u t it was m o v e d back a n additional 1.2 m d u r i n g the course of the experiment, apparently w i t h o u t affecting the b e h a v i o u r of the animals. The dim-red cage lights a n d a similar light h a n g i n g over the observer's head were t u r n e d o n during all observations, day as well as night. T u r n i n g o n the red lights did n o t arouse the

animals when they were sleeping, a n d it apparently did n o t excite t h e m or slow d o w n their activities when they were awake. White lights, if t u r n e d o n at night a n d left o n for a n y length of time, usually caused the animals to assume a sleeping posture at the back of the cage.

Results Daily Activity Cycles Figures 2 a n d 3 present the prevalence of selected activities over 24-hr periods. The animals slept from 06.00 to 17.00, woke u p

ANIMAL

666

BEHAViOUR,

17,

X-------X

NON-SLEEPING, NON-LOCOMOTORY

0 ....

SLEEP

0

,

4

POSTURES

-_- L O C O M O T I O N

IO0

,o-~

90 09 Z 0

70t.LI O9 m 0 I-Z ILl

I I I I

80

60. 50-

,x, "~'~ d'!!

!"x d)c

ii

!

I

.".

ILl fl

I

oiD ,,/ &J

_ i,

/~,,.: " ~\ o,,_ /\,, I0.

0

I

600

A

\

7t "7 ' 27 .<"; ,"t, F;

"~ I

9

,'it i I

1200 CLOCK TIME

L~

I

I

1800

24.00

Fig. 2. Diurnal changes in sleep, locomotion and non-sleep, non-locomotion postures.

25

--

x x INGESTION ~ - - o GROOM ~ IERINEAL. RUBBING

Q

e

:

2O 03 Z 0 > n," h, 09 m 0 I-Z I,I 0 n." hi O.

15

10--

0

600

1200

1800

2400

CLOCK TIME Fig. 3. Diurnal changes in grooming, ingestion and perineal rubbing.

T E N A Z A et al.: B E H A V I O U R A N D ACTIVITY RHYTHMS O F SLOW LORISES PLATE

XV

Fig. 1. The experimental situation: A, behind the observer's screen; B, the cage battery; C, an individual cage. Tenaza et al., Anim. Behav., 17, 4

PLATE

XV1

Fig. 4. Illustration of behaviours; A, climbing; B, walking; C, perineal rubbing; D, sitting sleep posture; E, upright sitting, awake; nonlocomotion posture; F, holding food with hand. Tenaza et al., Anim. Behav. 17, 4

TENAZA et al. : BEHAVIOUR AND ACTIVITY RHYTHMS OF SLOW LORISES between 17.00 and 18.00, and engaged in wakeful activities during the 12 hr between 18.00 and 06.00. The onset of activity at about 18.00 was coincident with the advent of night light conditions within the building. Individual activities are discussed in the following paragraphs. Locomotion

We include only walking and climbing under the rubric of locomotion. An animal pacing on the floor of the cage was considered to be walking, and one locomoting on a wall or the ceiling of its cage was considered to be climbing (Plate XVI, Figs. 4A and B). The two activities occurred with equal frequency, but locomotion was observed 2.1 times more often in males than in females. R u b b i n g P e r i n e a l R e g i o n on F l o o r

All of the lorises were observed rubbing their perineal regions against the cage floor while walking distances of a few centimetres to 2 m (Plate XVI, Fig. 4C). Perineal rubbing accompanied walking 24 per cent of the time in males and 39 per cent of the time in females (overall 28 per cent). We saw perineal rubbing occur only on the cage floor, never on ceiling or wall, but as Table II shows, it was not confined to a particular part of the floor by any animal. Among prosimians, perineal rubbing has been reported in males of the slender loris by Ilse (1955) but not by Subramoniam (1957); in males of Galago senegalensis (Sauer & Sauer 1963) and in both sexes of Tupaia glis (Kaufmann 1965).

66;]

On thirteen of the fifteen occasions that cages were examined after seeing animals perineal rubbing, drops of urine were found adhering to the cage floor along the path the animal had taken. This indicates that urine deposit may be a regular part of this behaviour in N. coueang as Ilse (1955) found it to be in the slender lofts. A male slow lofts was also observed to defaecate and then immediately drag his rump across the cage, a phenomenon reported in tree shrews by Kaufmann (1965). Hill (1953) states that 'All lorisoids have a strange habit of washing their hands by micturating on them.' Although 'urine washing' has been reported in Nyeticebus (Hill 1938), as well as in the genus Loris (Hill 1938; Ilse 1955); and Galago (Hill 1938; Sauer & Sauer 1963), we did not observe the activity in our slow lorises. Either it was not a part of their repertoires, it was quelled by the conditions under which they were kept, or we simply overlooked the behaviour. The last possibility seems rather unlikely, since, judging from other authors' descriptions, it is not an inconspicuous activity. Sleeping

The animals slept either sitting (Plate XVI, Fig. 4D) or lying on back, side or belly. Animals in the sitting attitude often held the head turned away from the midline, resulting in an asymmetrical posture. The sitting posture was observed 78 per cent of the time and the lying down posture 22 per cent of the time. One animal was never observed lying down, and another was seen doing so only twelve times (Table I).

Table II. Location of Perineal Rubbing Within the Cage

No. of times observed for animal number Floor location

1

2

3

4

5

Near left front corner

1

0

0

1

0

0

Near right front corner

1

1

0

0

1

2

Near right rear corner

0

1

1

0

0

0

Near left rear corner

0

2

1

1

4

0

Near front wall

2

3

2

0

9

6

Near right wall

3

4

0

1

3

9

Near rear wall

1

0

2

2

6

4

Near left wall

1

4

I

0

3

2

Near centre o f cage

2

3

1

0

5

2

66g

ANIMAL

BEHAVIOUR,

The frequency of lying down increased during the afternoon hours, perhaps reflecting the increased temperature in the animal house. Stretching out increases the amount of body surface over which heat loss can occur. MacKenzie (1929) noted that his slow loris usually slept 'rolled in a ball' but that it stretched out in hot weather. Table III presents the frequencies with which we observed sleeping postures at different intracage locations. Most striking is the fact that 96 per cent of the time animals in sleeping postures were in one of the rear corners of the cage. Furthermore, all but one animal spent a substantially greater amount of time in one rear corner than in the other. Hediger (1950) has indicated, and we observed, that the slow loris is disturbed by light, and it may be for that reason that our animals chose to sleep in the rear, darker, portion of the cages. That they slept in corners suggests a tendency to maximize contacts of the body with environmental surfaces while sleeping. Non-sleeping, Non-locomotory Postures This category includes those postures assumed by animals that were neither locomoting nor in a sleeping attitude. Most frequent among these was the dog-type sitting posture back on the haunches with the arms more or less straightened to elevate the anterior end of the body (Plate XVI, Fig. 4E). This accounted for 62 per cent of our observations on non-locomotory postures (Table I). Next, at 21 per cent, was standing upright with hands on the cage wall. The remaining three postures, sitting with hand(s) on a cage wall, standing erect on all fours and

17,

4

crouched on all fours accounted, respectively, for 6 per cent, 9 per cent and 3 per cent of our observations. Females were observed in non-sleeping, nonlocomotory postures 44 per cent more times than were males. This is correlated with the greater amount of locomotion and slightly less sleep in the male group (Table I).

Self-grooming According to Hill (1953) all lorises, as well as all galagos and lemurs, groom by licking the fur, 'combing' the fur with the mandibular teeth and scratching with the claw on the second pedal digit, which, he points out, 'is able to reach parts inaccessible to the tongue and teeth.' We observed licking and scratching but not 'combing', and this is similar to Subramoniam's (1957) description for slender lorises. We also observed a grooming activity not mentioned by Hill, but described by Sauer & Sauer (1963) for Galago, viz., wiping the face with the hands after these had been licked. The claw was often licked right after being used for scratching, as Jolly (1967) has observed in lemurs. Lowther (1939) observed a Galago crassicaudatus which, after scratching, 'cleaned his paw by putting it in the side of his mouth'. We tallied direct licking of the extremities or trunk 413 times (89 per cent) and scratching with the claws 40 times (11 per cent). Wiping the face with licked hands did not occur at the moment of any of our tallies. We observed 57 per cent more grooming among the females than among the males (Table I). The animals were free of ectoparasites and

Table HI. Sleeping Locations Within the Cage No. of times observed for animal number: Location

1

2

3

4

5

6

Near left front corner

3

0

0

0

2

0

3 157 318 1 3 2 18 10

0 210 197 0 0 0 0 0

8 53 312 0 0 15 0 4

1 360 9 1 1 7 0 0

0 314 131 0 0 0 0 0

0 176 243 0 0 0 0 0

Near right front corner Near right rear corner Near left rear corner Near front wall Near right wall Near rear wall Near left wall Near centre of cage

TENAZA et al.: BEHAVIOUR AND ACTIVITY RHYTHMS OF SLOW LORISES sores which might otherwise grooming frequencies.

have affected

Ingestion H i l l (1953) states, with reference to drinking: 'True lemurs lap with their tongues, but lorises dip their hands in the fluid and lick them dry afterwards.' Similarly, Crandatl (1964) says that the slow loris drinks milk by 'licking it from its fingers in the usual style of the family'. However, only one of our six animals drank like this fairly regularly; it was tallied licking milk from its hand eighteen times ( = 62 per cent) and lapping from the bowl, catlike, eleven times ( = 38 per cent). Another animal was seen licking milk from its hand one time, but none of the remaining four animals were ever observed doing so (Table I). Rather, they always lapped up their milk in a cat-like fashion, as do slender lorises (Subramoniam 1957), Galagos (Lowther 1939; Sauer & Sauer 1963) and the Lemuroidea (Hill 1953). The lorises had three ways of handling solid food (i.e. bananas) while eating it. They would hold it up off the floor with one or both hands (Plate XVI, Fig. 4F), leave it on the floor with one or both hands on it or leave it on the floor without touching it with the hands. These were tallied six, two and five times respectively.

Discussion The picture of Nycticebus coucang as a nocturnal, light-shunning animal with a simple behaviour repertoire relative to monkeys was confirmed in this preliminary study. The data indicate that even when food is freely available, the slow loris remains active throughout the night with no important changes in the prevalence of any particular behaviour as the hours progress. Although light intensity is probably the main variable determining general activity level it would be worth while asking whether, with light constant, an endogenous rhythm would be evident. Considering that different situations were used, the similarity of the behaviour of the slow loris in this experiment with that of the slender loris reported by Subramoniam (1957) is remarkable. Until a more adequate comparison in a common environment is done no conclusion should be made. However, it presently appears that the behavioural data do not support the division of these animals into separate genera, despite their slight morphological differences and their geographical separation.

Summary Th.e behavio.ur of six ~ndividuall.y caged adu!t~

669

Nycticebus coucang, including three of each sex, was studied in Thailand. Locomotion, sleeping and non-sleeping postures, grooming and ingestive activities are described, quantified, and illustrated with photographs. The lorises slept in the darkest part of their cages during the day and engaged in wakeful activities at night. Males walked and climbed twice as much as females, and females groomed 57 per cent more than males. A behaviour which is possibly olfactory marking, two sleeping postures, five nonsleeping postures, three grooming methods, two ways of drinking and three means of handling solid food are described and their frequency in laboratory cages noted.

Acknowledgments The study was supported in part by a grant from the Division of Research Facilities and Resources, National Institutes of Health (FR00164). Kathy Tenaza helped with the data analysis and D r John T. Emlen improved the manuscript.

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Jolly, A. (1967). Lemur Behavior: A Madagascar FieM Study. Chicago: Univ. of Chicago Press. Kanfmann, J. H. (1965). Studies on the behavior of captive tree shrews (Tupaia glis). Folia Primatol., 3, 50-74. Lowther, F. de L. (1939). The feeding and grooming habits of the Galago. Zoologica (N. IT.), 24, 477480. MacKenzie, J. M. D. (1929). Food of the slow loris (Nycticebus coucang). J. Bombay nat. Hist. Soc.,

33, 971. Pournelle, G. H. (1955). The bashful clown. Zoonooz, 28, 23-25. Sanderson, I. T. (1957). The Monkey Kingdom. London: Hamish Hamilton. Sauer, E. G. F. & Sauer, E. M. (1963). The south-west African bush-baby of the Galago senegalensis group. Jl. S. W. Africa scient. Soc., 12, 5-35. Subramoniam, S. (1957). Some observations on the habits of the slender loris, Loris tardigradus (Linnaeus). or. Bombay nat. Hist. Soc., 54, 387-398. Washburn, S. L. & Hamburg, D. A. (1965). The study of primate behavior. In Primate Behavior (ed. I. DeVote). New York: Holt, Rinehart & Winston. (Received 2 August 1968; revised 15 April 1969; M.S, numb~er; A732)