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Behavioral characterization of sleep in stumptail macaques (Macaca arctoides) in exterior captivity by means of high-sensitivity videorecording.

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American Journal of Primatology 36245-249 (1995)
Behavioral Characterization of Sleep in Stumptail
Macaques (Macaca arctoides) in Exterior Captivity by
Means of High-Sensitivity Videorecording
JAIRO MUNOZ-DELGADO'.', GUSTAVO LUNA-VILLEGAS3, RICARDO
M0NDRAG6N-CEBALLOS1.', AND AUGUST0 FERNANDEZ-GUARDIOLA3.4
'Department of Ethology, Instituto Mexicano de Psiquiatria and 2Psychobiologyand
Behavior Unit, Centro de Neurobiologia, UNAM; 3Laboratoy of Sleep, Division of
Neurosciences, Instituto Mexicano de Psiquiatria, and 4Facultad de Psicologia,
UNAM, Mexico City, Mexico
There are reasons to consider incomplete the description of sleep in many
non-human primate species. Recording animals by highly sensitive videos
to obtain detailed descriptions of nighttime behavior and evidence of muscle activity while in a resting posture, seems a promising approach to the
non-invasive study of sleep in non-human primates. The present work
describes the use of ultrasensitive videocameras to record and analyze
spontaneous nighttime behaviors in captive non-human primates. Its
main purpose is to emphasize the utility of videorecordings to analyze
nighttime behavior. A heterosexual group of nine stumptail macaques ( M .
arctoides) was studied. It was possible to identify resting postures: immobility or lying on the floor as well as sleep movements and behavioral
signs of sleep. This procedure permits recognition of each animal individually and the data suggest that videorecordings, among other techniques
available, may be a useful, non-invasive method to study sleep.
0 1995 Wiley-Liss, Inc.
Key words: sleep, macaques, videorecording, behavior
INTRODUCTION
There are reasons to consider incomplete the description of sleep behavior in
many non-human primate species. Among these are the logistic problems of locating and monitoring sleeping sites in the wild, and the poor visibility in the dark,
leading to a n understandable bias to study daytime behavior [Anderson, 19841.
Research using captive animals with suitable observation methods (for example, by means of infrared illumination) may partially overcome these problems and
enhance the understanding of primate sleeping habits. Recording animals with
infrared or highly sensitive videos may make possible detailed descriptions of
nighttime behavior and provide evidence of muscle activity while in resting pos-
Received for publication April 20, 1994; revision accepted September 27, 1994.
Address reprint requests to Jairo Munoz-Delgado, Departamento de Etologia, Division de Investigaciones en Neurociencias, Instituto Mexicano de Psiquiatria, Antigua camino a Xochimilco 101, Colonia
San Lorenzo Huipulco, Delegation Tlalpan, C .P. 14370, Mexico, D.F., Mexico.
0 1995 Wiley-Liss, Inc.
246 / Munoz-Delgadoet al.
TABLE I. Age (inYears) and Sexes of the Stumptail Macaques, and
Time (in Minutes) Each Animal Was Videorecorded
Subject
PE
HI
GR
FR
TI
cu
VI
TO
ES
Age in
years
12.4
17.7
16.7
7.6
16.3
3.8
8.8
16.0
1.2
Category*
Age
Sex
Time
recorded
M
F
F
M
F
F
M
M
M
347.5
267.1
327.6
328.6
293.6
348.6
315.5
315.5
319.5
*The categories are as follows, age: Infant (I), Juvenile (J),Subadult (S),Adult (A), and for
sex: Male (M),
Female (F).
tures. This would represent a promising approach to the non-intrusive study of
sleep in non-human primates and has been used in studies of adult human beings
[Hobson & Spagna, 19781, children [Szymczak et al., 19931, and cats [Herman et
al., 19911.
The present work describes the use of ultrasensitive video cameras to record
and analyze spontaneous nighttime behaviors in captive non-human primates.
These videocameras require as little as 1.5 lux to yield more than acceptable
images. The main purpose of this paper is to emphasize the utility of videorecordings to store and analyze nighttime behavior. Thus, we limit ourselves to describe
quantitatively the resting behavior shown during the night.
METHODS
Animals and Housing
A heterosexual group of nine stumptail macaques (M. arctoides) housed in the
Department of Ethology of the Instituto Mexican0 de Psiquiatria, was studied.
Table I shows the sex and ages of the subjects, and the total time each was videotaped. The details concerning the animals’ origin and purposes of the colony have
been published elsewhere [Estrada & Estrada, 1981; Diaz, 1985; Lopez-Lujan et
al., 19891.
Recording Conditions
A highly sensitive, television closed-circuit that works with as little a 1.5 lux
was used (Elbex remote control camera EX6942 and monitor EXM1207). The images were stored on magnetic tape. For 15 nights before the beginning of the study,
the subjects were habituated to an all-night faint red light illumination of the cage
(one 40-watt light bulb), which was required for the filming. The lights were
turned on at the onset of darkness. The camera was placed in the center of the
observation area (Fig. 1)with the rest of the equipment kept within the laboratory,
thereby eliminating the possibility that the animals would react to the observers.
Recordings began a t 1900 h and ended at 0700 h. The filming sessions were done
on different nights throughout the summer of 1991. Each filming period lasted for
two hours with two-hour resting intervals between each session. Although the
beginning of recording hour varied each night in relation to the sunset, the entire
night period was covered. Thus, three sessions, six hours each, were completed
Sleep in Stumptail Macaques I 247
U
I
V I E W OF THE C A G E S
Fig. 1. Aerial drawing of the cages of the non-human primates colony. Cage 2 was the one studied here. The
videocamera was put in front of the window facing the cage, while the recorder, the monitor, and the button
panel that controls movements and focus of the camera were placed inside the laboratory.
each night, yielding a total of 18 h of videorecordings. In average, each animal was
recorded for 318.2 (8.5 SEMI minutes (Table I). The data are presented as frequencyhour rates (Table 11).
RESULTS
From the video recordings, it was possible to identify such resting postures as
either immobility or lying on the floor. The sleeping posture described by Bertrand
119691 was also identified. The frequency per hour of behaviors related to sleep are
shown in Table 11. The following categories specifically related t o nighttime activity were added to our ethogram of the species:
Sleep movements. Actions such as changing posture, opening eyes, closing
eyes, rocking, standing up and startle-like responses.
Behavioral signs of sleep. These were mainly myoclonus, muscle atony,
slow eye movements, and being still for more than 15 minutes. When not sleeping,
the animals self-groomed, groomed another individual, and even behaved aggressively. Also, it was found that observers were capable of identifying individuals as
accurately as in daytime (Table 2, Fig. 2).
DISCUSSION
This is a preliminary analysis of nighttime behavior of stumptail macaques; a
brief presentation of the exciting and promising data to be gathered throughout
the night. So far, our results show that besides being able to recognize subjects in
the darkness, and record subtle movements that occur during sleeping (such as
myoclonus or slow-eye movements), the stumptails do not sleep throughout the
night period, but display other behaviors.
We expect that in ongoing recordings we will be able to recognize behaviorally
248 J Munoz-Delgadoet al.
TABLE 11. Behaviors Observed During Nighttime
Sleep
postures
movements
Behavioral
signs of
sleep
Subject F" ~ / %=
h ~F" ~ / %c
h ~F"
PE
HI
GR
FR
TI
cu
VI
TO
ES
15
11
8
5
3
3
8
6
2.6
2.5
1.5
.91
.61
.52
1.5
1.1
1 .19
16
11
17
10
3
3
9
10
1
12
9
7
6
27
7
37
17
4
2.1
2.0
1.3
1.1
5.5
1.2
7.0
3.2
.75
13
9
15
12
32
9
43
30
5
2
26
6
6
17
11
13
7
5
~
h
.34
5.9
1.1
1.1
3.5
1.9
2.5
1.3
.93
Selfdirected
Grooming
%c
b
F"; ~ / h
%' ~F"
2
26
13
12
20
14
15
12
6
14
21
13
13
19
30
2
3
28
2.4
4.7
2.4
2.4
3.9
5.2
.38
57
5.3
15
21
28
27
23
39
2
5
39
41
30
23
11
11
24
24
20
30
Aggressive
~ / h b %c
7.1
6.7
4.2
2.0
2.2
4.1
4.6
3.8
5.6
F" FM
%=
43 11 1.9 10
30 2 .44 1
50 11 2.0
23
23 1 .18 2
13 6 1.2
7
31 2 .34 24
28 0
36 2 .40 3
41 5 .90 6
"F: Frequency; bFh: Frequencyhours of recording; '%: percent of time behavior was observed
Fig. 2. Still-pictures of the videos allowed to identify individuals.
the REM and non-REM phases of sleep, a s well as to detect whether the stumptails
show sleep disorders, such as insomnia or hypersomnia, known to occur in human
beings.
Moreover, the image resolution of the filming was good enough to recognize
each animal individually, even when freezing the images (Fig. 2); of course, the
T.V. image greatly improves when the video is running.
Finally, we would like to stress the utility of videorecordings among other
techniques available, such as time-lapse photographs [Hobson & Spagna, 1978;
Herman et al., 19911, and verbal-report questionnaire [Szymczak et al., 19931 as
Sleep in Stumptail Macaques / 249
non-invasive methods in sleep studies. Many commercial video equipments have a
quite satisfactory sensitivity and resolution in dim light settings allowing the
researcher to film the wandering and shifts in postures of recognized individuals
[Hobson & Spagna, 1978; Herman et al., 19911 and also short lasting movements
of small areas of the body surface.
CONCLUSIONS
1. This non-invasive videorecording method is suitable for the study of sleep in
non-human primates, both captive and in the wild.
2. It is possible to obtain accurate images going from the recognition of individuals, particular resting postures and subtle movements, such as myoclonus and
eye movements.
ACKNOWLEDGMENTS
The study was supported by Instituto Mexican0 de Psiquiatria and the Programa Universitario de Investigacion en Salud PUIS-UNAM, key 3330. We thank
anonymous referees for their comments, Raul Cardoso for help with illustration
and drawing work.
REFERENCES
Anderson, J . Ethology and ecology of sleep
in monkeys and apes. ADVANCES IN
THE STUDY OF BEHAVIOR. New York,
Academic Press, 1984.
Bertrand, M. THE BEHAVIORAL REPERTOIRE OF THE STUMPTAIL MACAQUE.
New York, S. Karger, 1969.
Diaz, J.L. Grupos no manipulados de primates cautivos como modelos en la investigacion psiquiatrica. SALUD MENTAL
8167-74, 1985.
Estrada, A.; Estrada, R. Reproductive Seasonality in a free-ranging troop of stumptail macaques (Macaca arctoides): a five
year report. PRIMATES 22503-511,1981.
Herman, M.; Denlenger, S.; Patarca, R.;
Katz, L.; Hobson, J . Developmental phases
of sleep and behaviour in a cat mother-in-
fant system: A time-lapse video approach.
CANADIAN JOURNAL OF PSYCHOLOGY 45101-114, 1991.
Hobson, A.J.; Spagna, T.; Malenka, R. Ethology of sleep studied with time-lapse photography: postural immobility and sleep
cycle phase in humans. SCIENCE 2-1:
1,251-1,253, 1978.
Lopez-Lujan, A.X.; Ramirez-Ochoa, I.; Mayagoitia, L.; Mondragon-Ceballos, R. Sex differences in intra-group spacing behaviour
in stump-tailed macaques (Macaca arctoides). FOLIA PRIMATOLOGICA 52:
102-108, 1989.
Szymczak, J.T.; Jasinska, M.; Pawlak, E.;
Zwierykowska, M. Annual and weekly
changes in the sleep-wake rhythm of school
children. SLEEP 16-5433-435, 1993.
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