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Behavioral contrasts between male cynomolgus and lion-tailed macaques.

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American Journal of Primatology 29:49-59 (1993)
BRIEF REPORTS
Behavioral Contrasts Between Male Cynomolgus and
Lion-Tailed Macaques
A. S.CLARKE* AND D. G. LINDBURG
Center for the Reproduction of Endangered Species, Zoological Society of San Diego, San
Diego, California
Evidence indicates that primate species differ not only in social structure
and concordant social propensities, but also in their approach toward novel
objects, environments, and procedures. These differences in response dispositions have been described as being based on differences in characteristic stances toward the environment, also called temperaments. This
report extends previous comparative primate research by describing behavioral contrasts observed among males of two macaque species, liontailed and cynomolgus macaques. The lion-tails demonstrated more interest in other animals, more vigilance and instrumental behavior, and more
readily adapted t o training to enter a small and unfamilar cage than the
cynomolgus. These results suggest temperamental differences between the
two species. Lion-tails may be characterized as bold, curious, and instrumental in their approach to the environment, while cynomolgus may be
characterized as more passive or "reserved." These differences may form
the basis for the well-developed sensorimotor abilities observed in liontails such as the manufacture and use of tools, and may also be related t o
their highly omnivorous diet. o 1993 Wiley-Liss, Inc.
Key words: species differences, temperament, manipulative behavior,
sensorimotor ability, Macaca silenus, Macaca fascicularis
INTRODUCTION
Evidence is accumulating that closely related primate species show differences
in proclivities toward engaging in certain types of behaviors, even where behavioral repertoires are highly similar [Clarke & Mason, 1988;Mason et al., in press].
Given the variety of social structures observed within the primate order, such
differences might be expected to be most apparent under social conditions. Indeed,
a number of studies have found distinct contrasts among primate species under
various social conditions or social challenges [e.g., Anzenberger et al., 1986; Caine
& Mitchell, 1980; Cubicciotti & Mason, 1975; Cubicciotti et al., 1986; Davis et al.,
1968; Hawkes, 1970; Mason et al.,in press; Mendoza & Mason, 1986; Small, 19821.
Similarly, other comparative primate studies have noted differences in nonsocial
activity profiles, such as use of space, foraging patterns, and time spent in loco-
Received for publication March 10, 1992; revision accepted July 10, 1992.
Address reprint requests to A.S. Clarke, Harlow Primate Laboratory, University of Wisconsin, 22 North
Charter Street, Madison, WI 53715.
0 1993 Wiley-Liss, Inc.
50 / Clarke and Lindburg
motion, vigilance, self-directed behavior, etc. [Andrews, 1984; Caine et al., 1981;
Davis et al., 1968; Fragaszy & Mason, 1983; Kawata, 19801. Some of these differences have been related to dietary and habitat differences in the wild [Caldecott,
1986; Fragaszy & Mason, 1978, 1983; Glickman & Sroges, 1966; Parker, 19741.
While responses to the nonsocial environment might be predicted to show less
obvious contrasts between species, several studies have noted behavioral differences among primate species in nonsocial test situations. The most common of
these have involved responses to novel objects. In the largest study, Torigoe [1985]
compared object manipulation among 74 primate species. He found a large range
of interspecific variation in degree and complexity of object manipulation, with the
apes, Cebus species, and macaques the most manipulative. Similarly, Parker
[1974] compared ten primate species in degree of object manipulation and found
that great apes showed the most frequent and diverse manipulative actions.
Other studies have sought to characterize differences among primates toward
novel stimuli beyond simply the degree of exploratory or manipulative behavior
exhibited. Glickman & Sroges 119663 compared novel object responses among 24
primate species and found that baboons and macaques were the most responsive
and were characterized as “highly reactive,” “aggressive,” and “vigorous” in their
approach toward the objects. Singh & Manocha 119661 found contrasts between
langurs (Presbytis entellus) and rhesus monkeys (M. muluttu) in their responses to
a variety of objects. Langurs were more bold and less fearful than rhesus, approached and contacted the objects more often, and showed less abnormal behavior.
Rhesus were also found to differ from gibbons (Hylobutes lur and H . pileatus) in
response to novel stimuli. Gibbons were more active, manipulative, and bold in
their approach toward unfamiliar objects, animals, and environments, while
rhesus showed more disturbance behavior [Bernstein et al., 19631.
These species differences have been characterized as response dispositions or
temperaments [Higley & Suomi, 1989; Kagan, 1989; Mason et al., in press; Mendoza & Mason, 19891, which may be described in relation to stimuli as attributes
such as “habituation, persistence, boldness and distractability” [Cubicciotti et al.,
19861. For example, in comparisons of two New World species, squirrel (Suimiri
sciureus) and titi monkeys (Cullicebus rnolloch) in response to various challenges,
Suimiri were characterized as more active, more “opportunistic,” “impulsive,” and
‘%older”than Cullicebus [Mendoza & Mason, 1984,19861.A recent report comparing responses of a New and an Old World species (Cebus upellu and M.fasciculuris)
to a highly salient artificial stimulus (a snake model) also illustrates temperamental differences in responses to this provocative stimulus. The cebus monkeys engaged in more approaches, exploratory behavior, and contact with the snake model
than the macaques, whose behavior toward the model was characterized by avoidance and fearful behavior. The authors suggested that these differences were based
on contrasts in predator defense and foraging strategies in the wild, which were in
turn related to the temperaments of the two species [Vitale et al., 19911.
Among the genus Mucacu, only a few species are well studied, and the number
of directly comparative studies is limited. While superficially similar in social
structure, these congeneric species do exhibit differences in aspects of social and
sexual behavior [reviewed in Melnick & Pearl, 1987; Shively et al., 19821. In a
series of laboratory studies, females of three macaque species (M.rnuluttu, M.
mdiutu, and M . fusciculuris) were compared in their psychophysiological responses
to several novel situations. The species showed striking contrasts in behavioral
and physiological responses to a novel environment [Clarke et al., 1988al and to a
simple operant training task [Clarke et al., 1988bl. In both situations, M. muluttu
were characterized as the most active and instrumental in their approach toward
Male Macaque Behavior / 51
the situations, M.radiuta as the most passive and least disturbed, and M. fascicularis as most disturbed. These differences were interpreted as based on temperamental factors that contrasted between the species [Clarke et al., 1988a,b].
Here we describe behavioral contrasts observed between males of two macaque
species, lion-tailed macaques (M. silenus) and cynomolgus macaques (M. fascicularis), while housed individually and in response to a simple operant training task.
Cynomolgus are relatively well known, but there have been few studies of the
endangered lion-tailed macaque. Both species are arboreal, omnivorous, nonseasonally breeding, and live in mixed agehex groups. Cynomolgus occupy a wide
variety of habitats throughout Asia [Richard et al., 19891. Lion-tails appear to be
restricted to primary forest [Green & Minkowski, 1977; Johnson, 19851, although
their now-limited range and endangered status make it diffieult to assess the
possible diversity of their true natural habitats [Vijayan, 19851.
METHODS
Subjects
The subjects were five adult male cynomolgus macaques (Macaca fmcicularis)
and five adult male lion-tailed macaques (M.
silenus). Ages ranged from 10-15 yrs
for the cynomolgus and 7-14 yrs for the lion-tails. All monkeys were believed to be
captive-born. The animals were housed in identical individual outdoor run cages (2
x 3 x 4m) in an off-exhibit facility at the Zoological Society of San Diego. The
animals were housed such that individuals of each species were in adjacent cages
with opaque side walls and the groups were directly across from each other. Thus,
conspecifics could not see each other, but each had direct visual access from the
front of cage to a member of the other species opposite (approximately 1.5 m apart,
separated by a walkway). All of the animals also had limited visual contact with
a large group of lion-tailed macaques housed nearby. Wire sitting platforms
(perches) were located at approximately one-half the cage height at the rear of each
cage. The front of the cages were equipped with a plastic shelter box (1 x 1 x
1.5m) that could be entered from a side door. The shelter box was mounted approximately 3 m off the floor, and the top of the box thus provided the most
elevated perch in the cage. The cages were roofed, and the floors were covered with
hay. Hay was changed and the cages cleaned on a weekly basis. The animals were
fed h i t s , vegetables, and commercial primate biscuits daily, and had water available ad libitum.
Procedures
Undisturbed condition. Behavioral data were collected from the subjects in
their individual run cages by the first author from a distance of 1m from the cage
front. Behaviors measured included locomotion, vocalization, feeding, foraging in
the hay substrate, environmental exploration, self-grooming, vigilance [defined as
being at the cage mesh with gaze directed outward, Caine et al., 19811, and facial
displays directed at animals caged nearby or the observer (threats, lipsmacks,
bared-teeth displays, and yawns). In addition, use of space and structures within
the cage was recorded. Stationary use of three locations (sitting or standing on>
was recorded: on top of the nest box at the front of the cage (a location providing the
best view of other animals); on the elevated perch at the rear of the cage (from
which no animals were visible); or, on the floor (where some animals might be
visible, depending on the subject’s location on the floor). Behavioral data were
collected between 9:OO-11:OO AM for 20 min per subject, 3 days a week for 5 weeks.
Within species groups, behavioral data from individuals were collected in preas-
52 / Clarke and Lindburg
signed random order. Testing order and times were balanced across species groups.
Behavioral data were recorded via one-zero sampling [Altmann, 19741,using 20
sec intervals.
Portable cage entry training. In this condition, the subjects were trained to
enter a portable metabolism cage voluntarily from their home cages, in order to
later collect urine samples for hormonal analysis as part of another study. During
training trials, the portable cage was attached by clips and chains to the wire mesh
of the subject’shome cage, and both cage doors opened. The subject was given 3 min
in which to enter the cage. If the monkey entered within the 3 min period, the
latency to enter (timed by stopwatch to the nearest second) was recorded. The
monkey then received a food reward and was confined in the cage for 5 min. If a
monkey did not enter within the 3 min interval, the cage doors were closed and the
trial was terminated. All subjects received five trials per day, one trial at a time,
with subjects tested in random order. Criterion for successful training was considered to be five consecutive voluntary entries within the three-minute interval
[Clarke et al., 1988bl. All subjects received 50 training trials, although all subjects
met criterion at between 30-45 trials. The ability to view group-housed lion-tails
(including females) not visible from their home cages but easily viewed from the
metabolism cages also provided a social incentive for entering the portable cages.
Data collected on training performance allowed for comparison of the two species
in their responses to these procedures.
Data Analysis
Interspecific comparisons of behavioral measures were made by MannWhitney U tests. Comparison of cage training latencies was made by an independent t test. The distribution of cage entries vs. refusals among the two groups was
evaluated by a Fisher’s exact test.
RESULTS
Three behaviors differed substantially between the two species in the solitary
condition. Lion-tails engaged in significantly more vigilance behavior (looking out
of the cage) than the cynomolgus (Fig. l A , U = 3.0,P = .04).Lion-tails also foraged
in the hay substrate more frequently that the cynomolgus(Fig. lB,U = 0,P = .009).
In contrast, the cynomolgus monkeys self-groomed more frequently than the liontails (Fig. lC, U = 3.0,P = .04).The two groups also differed in utilization of locations within the cage, showing symmetrically opposite patterns in use of the two
arboreal cage structures. Lion-tails were observed significantly more often than
cynomolgus on top of the shelter box (U= 2.0, P = .03),whereas cynomolgus spent
significantly more time than lion-tails on the elevated perch W = O , P=.OO9).
These data are shown in Figure 2. There was no difference between the groups in
time spent on the floor. There were also no significant differences for the other
solitary behaviors recorded (locomotion,vocalization, feeding, and environmental
exploration), nor in facial displays directed at nearby animals or the observer.
In the cage training condition, the two species showed consistent differences in
performance on the task of voluntarily entering the portable cage within the required interval. .As shown in Figure 3, average latency to enter was consistently
longer for the cynomolgus over all training trials (t = 6.1, P=.OOl). A second
measure of training performance, the number of refusals to enter vs. voluntary
entries, was also greater for the cynomolgus (P=.03,Fisher’s test). This result is
shown in percentage form in Figure 4.
Male Macaque Behavior I 53
‘OW
1
I
H
LTM
m
VIGILANCE
8o
1
B
2o
1
HAY FORAGE
SELF-GROOM
Fig. 1. Mean frequency of display of the behaviors (A)vigilance, (B)foraging in the hay substrate, and (C)
self-grooming in male lion-tailed (LTM) and cynornolgus (CYN) macaques.
54 / Clarke and Lindburg
LTM
CYN
-r
40
Z
W
3 30
CI
W
K 20
LL
10
0
SHELTER BOX
PERCH
Fig. 2. Mean frequency of sitting or standing on the elevated structures in the cage, perch and shelter box.
iz
+.
A
--
E
0’
LTM
CYN
I
I
I
I
I
I
I
I
I
I
5
10
15
20
25
30
35
40
45
50
TRIALS
Fig. 3. Mean latency to voluntarily enter a portable metabolism cage over 50 training trials.
DISCUSSION
Several striking behavioral contrasts between the lion-tail and cynomolgus
groups were demonstrated under these conditions. Lion-tails engaged in much
more frequent vigilance and manipulation of the hay substrate than the cynomolgus. In contrast, the cynomolgus showed more frequent self-grooming behavior.
The lion-tails also entered the initially novel metabolism cage more often and
consistently more quickly than the cynomolgus during training. While in the metabolism cages, all animals could view animals not visible from within their single
cages, including two lion-tail groups containing females and young. This may have
provided a social incentive for entering the smaller cages [Fujita, 19871. The liontails’ performance during training suggests a more active approach and greater
“boldness’’ toward unfamiliar aspects of the environment for this species, and
perhaps a greater general interest in the outside environment and/or other animals. Differences between macaque species in an analogous procedure were also
interpreted as the result of interspecific differences in temperaments rather than
in learning ability [Clarke et al., 1988bl.Other comparative studies of learning in
Male Macaque Behavior / 55
loo
3
5
1
LTM
8o
60
40
8
20
0
REFUSALS TO ENTER
Fig. 4. Mean percent of trials in which animals refused to enter the portable metabolism cage within the 3 min
trial interval.
macaques have generated similar conclusions [Schrier, 1965; Symmes & Anderson, 19671.
All of these results suggest that the lion-tails were more oriented towards
external objects and events in their environment, and were the more “instrumental” of the two species. Manual manipulation of the hay substrate and vigilance are both forms of environmental exploration, although one is tactile and the
other visual. Other data suggest that lion-tails are a highly manipulative and
instrumental species, perhaps more so than other macaques [Westergaard, 19881.
In a previous study, lion-tails were found to be the most manipulative and exploratory of 13 macaque species, and to use the greatest variety of manipulations of
objects [Torigoe, 19871. M. fusciculuris were ranked fourth in both frequency and
variety of object manipulation in the same study.
Taken together, these behavioral tendencies suggest a greater “curiosity” toward the environment [Wood-Gush& Vestergaard, 19911 for the lion-tails than for
the cynomolgus. This tendency has been related to an omnivorous diet [Westergaard, 1988; Wood-Gush & Vestergaard, 19911, which in turn depends on welldeveloped exploratory behavior and a tendency to exploit foods which are embedded or otherwise require manipulation for acquisition [Gibson, 1986; Parker, 1973;
Parker & Gibson, 19771. Thus, lion-tails might be expected to be more omnivorous
and/or to make greater use of extractive foraging techniques in the wild. Data
indicate that lion-tails are highly omnivorous [Artaud, 1980; Johnson, 1985;
Green, 19761, probably more so than the more frugivorous cynomolgus [Wheatley,
19801. Whether lion-tails also utilize more manipulative and/or extractive foraging
techniques than cynomolgus is uncertain. However, the hay foraging data suggest
this, a8 do other data indicating advanced sensorimotor abilities [Torigoe, 1987;
Westergaard & Lindquist, 19871, and well-developedtool use in this species [Westergaard, 19881. Tool use has been linked to the use of extractive foraging techniques, since most animal tool use occurs in this context [Beck, 1990; Parker &
Gibson, 19771. Lion-tails have been observed to use tools in food preparation in the
wild [Hohmann, 19881 and for food acquisition in captivity [Westergaard, 19881.
Further, this is the only Old World monkey species in which a group of animals has
been observed to spontaneously manufacture and use tools [Westergaard, 19881.
The two species also differed in their use of space and structures: lion-tails
spent most of their time on the shelter box (the most arboreal cage structure),
56 / Clarke and Lindburg
while cynomolgus preferred the midlevel perch. While other animals could be
viewed from the top of the shelter box, none were visible from the perch. It is
unclear as to whether this result reflected a difference in height preference per se
or in the desire to view other animals. Both species are primarily arboreal, however, lion-tails are believed to be the most arboreal macaque species [Roonwol &
Mohnot, 19771. It is likely that the lion-tails preference for the shelter box reflected both their greater general vigilance tendency, and apparently greater motivation to view other animals. That the species did not differ in time spent on the
floor supports this interpretation. Other data from studies of multimale and onemale captive groups indicate that lion-tail males in these groupings also spend a
large proportion of their time in vigilant behavior, whereas group-living cynomolgus do not [Clarke, Harvey, & Lindburg, unpublished data).
Other studies have also found variation among macaques in vigilance. Davis
et al. [19681 found that rhesus engaged in considerably more vigilance than pigarctoides). Caine et al. [19811 found that
tails (M.nemestrinu) or stumptails (M.
rhesus showed much more vigilant behavior than bonnets (M.
radiata). This difference was ascribed to the fact that rhesus are the more aggressive, show less
interindividual tolerance, and are more likely to emmigrate. Thus, rhesus were
more often peripheral and vigilant, while bonnets directed their attention into
their more social groups. A similar explanation may account for these results.
Lion-tails show little or no intermale tolerance in captive groups and high levels of
agonism. In contrast, these cynomolgus macaques showed frequent ailiative behavior and low levels of aggression in social contexts. The greater self-grooming
exhibited by the cynomolgus may be related to their greater frequency of allogrooming in a group (Clarke & Lindburg, 1988 and unpublished data).
It is likely that the behavioral propensities found to differ between these two
species are based on more broad and general temperamental differences between
them. These observations may also be related to social, dietary andlor habitat
differences, which in turn may be based on phylogenetic divergence [Fooden,
19801. Probably all of these contribute to the species differences reported here in
response to objects and features of the physical environment. Available evidence
suggests that the lion-tailed macaque is unique among macaques in its welldeveloped instrumental and tool-using activity. The display of these abilities is likely
facilitated by the lion-tails’ bold and active approach toward novel aspects of the
environment.
CONCLUSIONS
1. These data extend previous comparative studies of macaques and demonstrate that males of two species differed dramatically in several aspects of behavior.
2. The behavioral differences observed appear to be based on temperamental
differences between the species in response to environmental stimuli. Lion-tails
may be characterized as bold and instrumental in their approach to nonsocial
stimuli, whereas cynomolgus are more passive and reserved.
3. Lion-tails appear to have the most advanced sensorimotor abilities of
macaques studied thus far, and these abilities are likely enhanced by their bold
and curious nature.
ACKNOWLEDGMENTS
We thank N. Harvey, D. Forster, and J. Malone for assistance in cage training,
and S. Mitchell for manuscript preparation. The research was supported in part by
Male Macaque Behavior / 57
NIH grant RR05481 to A. S. Clarke and D. G. Lindburg. Assistance was provided
by the staff and resources of the Wisconsin Regional Primate Research Center
library, which is supported by PHS grant RRO169-32.Portions of the manuscript
were prepared while A. S. Clarke was supported by the John D. and Catherine T.
MacArthur Foundation Mental Health Research Network I.
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