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American Journal of Primatology 24:61-66 (1991)

Possible Antipredator Behavior Associated With River


Crossings by Proboscis Monkeys (Nasalis larvatus)
CAREY P. YEAGER
Psychology Department, University of California, Davis

Proboscis monkeys (Nasalis laruatus) river crossing behavior was exam-


ined as a potential behavioral response to predation threat. N . laruatus
major predator at the Tanjung Puting National Park in Kalimantan Ten-
gah, Indonesia, appeared to be the false gavial (Tomistoma schlegeli), a
crocodilian. An adolescent female proboscis monkey was captured and
drowned by a false gavial during this study. The monkeys crossed the river
at its more narrow points, with several individuals or groups crossing
simultaneously. Increased vigilance prior to crossing and leaping as far
across the river as possible were also observed. Proboscis monkey groups
often associate at their sleeping sites at the rivers edge. A potential func-
tion of these associations may be to allow groups to synchronize their
movement with other groups during river crossings.

Key words: predation, Nasalis laruatus, intergroup movement patterns,


Tomistoma schlegeli, crocodilian
INTRODUCTION
Predation on nonhuman primates has rarely been documented [Cheney &
Wrangham, 19871. This paper focuses on one known predation of a proboscis mon-
key and possible antipredator behavior associated with river crossing by proboscis
monkeys. The data were collected during 1984-1985 as part of a study of the
proboscis monkeys social organization and ecology a t the Natai Lengkuas Station
in Tanjung Puting National Park, Kalimantan Tengah, Indonesia. Group struc-
ture, intergroup patterns of association, and some ecological concerns have been
addressed previously [Yeager, 1989a,b, 1990a,b, 19911.
The proboscis monkey (Nasalis Zaruatus), a member of the subfamily Colobi-
nae, is a large arboreal, sexually dimorphic species endemic to the island of Bor-
neo. Stable one-male groups are the principle social unit [Bennett & Sebastian,
1988; Yeager, 1989a, 1990al. These groups are further organized into bands with
fission-fusion between groups within bands [Yeager, 19911. All-male groups are
also present. Groups within the same band generally coordinate their movements
[Yeager, 19911.
Proboscis monkeys typically spend the majority of their time near water, re-
turning to the waters edge each evening to sleep. In riverine habitats, home

Received for publication July 10, 1990; accepted November 30, 1990.
Carey P. Yeager is now a t the Psychology Department, University of Tennessee, Knoxville, TN 37996-
0900. Address reprint requests there.

0 1991 Wiley-Liss, Inc.


62 I Yeager
ranges may encompass both sides of the river, making i t necessary for the animals
to swim [Bennett & Sebastian, 1988; Salter et al., 1985; Yeager, 1989al or, where
possible, leap across the river (Yeager, personal observation). Morphological fea-
tures such a s webbing between the fingers and toes [Schultz, 19421 and a sufficient
fat:muscle ratio make them proficient swimmers (Yeager, personal observation).
Clouded leopards (Neofelis nebulosa) [Davis, 19621 and a crocodilian, the false
gavial (Tomistoma schlegeli) [Galdikas, 19851, are the only documented predators
of N . laruatus, apart from humans. Monitor lizards (Varanus sp.) and snakes,
suggested as potential predators of long-tailed macaques [Fittinghoff & Lindburg,
19801, may also present a threat to proboscis monkeys.
METHODS
Subjects and Study Site
At least 12 groups of proboscis monkeys (ten one-male and two all-male
groups) were observed within the study site. Group sizes ranged from 3 to 23 (X =
12.1) a t the end of the study.
The primary study area was located along a 2 km stretch of the Sekonyer Kiri
river. The study area was a freshwater peat swamp that had been lightly hand
logged previously. The average canopy height was 11.4 m (some emergents
reached 25 m or more), with a partially discontinuous canopy near the river. The
swamp and river water level fluctuated greatly; the river level varied more than
2 m due to seasonal flooding. Further information can be found in Yeager [1989a,b,
1990a,b, 19911.
Data Collection and Analyses
Approximately 1,700 h of observation were made on proboscis monkeys during
group follows. Additional data were collected during 336 evening census surveys of
the study area and opportunistic observations. Event-sampling (also referred to as
all occasions sampling) [Lehner, 19791was used in recording predation, potential
predation attempts, and river crossings.
The average river width was determined by measurements made every 25 m
along a 2.5 km stretch that included the primary study area. Measurements were
also made at every known crossing site. Groups were often difficult or impossible
to identify when in the process of crossing the river; thus the data for crossing sites
were pooled. Since pooling increases the potential for error in statistical analyses,
frequency distribution data are also provided.
The number of river crossings per month was estimated for four groups (R, FB,
K, and GR) that were regularly observed over a 6 month period (July-December
1985); as only partial data from December 1985 were obtained, those data were not
used in calculating monthly averages. Estimates were based on known sleeping
site locations from evening census surveys, plus data from group follows and op-
portunistic observations. A group was recorded a s having crossed the river if 1)i t
was observed crossing or 2) it had been sighted previously on the opposite river
bank. This was a conservative estimate, a s i t was possible that a group might cross
to the opposite river bank and return before being sighted again. As proboscis
monkey groups often coordinate their general movement patterns with specific
other groups [Yeager, 19911, coordination of river crossing movement between two
or more groups was assumed to have occurred if the groups concerned were all
observed the previous evening on the opposite river bank. A group was assumed to
have crossed independently if it had been observed the previous evening on the
opposite river bank and other groups remained on the same river bank a s the
previous evening. It was not possible to sight or identify all groups every census
Proboscis Monkey Antipredator Behavior I 63
(groups moved out of the study area, and poor observation conditions could prevent
identification); thus many crossings were not assigned to either category (coordi-
nated or independent). Tentative assignment can be made based on the groups
locations with regard to the other groups prior to and after the cross. For example,
on day 1census groups K and GR are within 100 m on the same river bank, during
day 2 census neither group is observed, and on day 3 groups K and GR are within
100 m on the opposite river bank. This would tentatively be considered a coordi-
nated river crossing.

RESULTS
Predation b y a False Gavial
Prior to reliable identification of groups, an unidentified one-male group of
proboscis monkeys (adult male, six adult females, five infants, and two immature
animals) crossed the river by themselves on January 28, 1985, between 1716 and
1726 h. They appeared agitated (honks, squeals, and increased movement) and
moved over 400 m upstream along the rivers edge during the next 1.5 h. The group
had not moved more than 200 m along the rivers edge during the previous 11h.
At approximately 1840 h the body of an adolescent female proboscis monkey was
recovered 800 m upstream from where the animals had crossed. A false gavial
released the body upon the approach of my assistants canoe. The recovery was an
opportunistic event; the assistants were returning from an evening census survey.
They were not able to determine the size of the false gavial. It seems probable that
the body recovered was from the group being observed: 1) No other groups were
observed between this group and the camp site (950 m upstream from crossing
site); 2) there is no information available concerning Tomistoma schlegeli, but
other crocodilians have been reported to move their prey [Pooley & Gans, 19761; 3)
it was a fresh kill; and 4) the group was extremely agitated and moved several
hundred meters a t a time when they should have been settling down and entering
sleeping trees.
The adolescent female appeared to have been in good condition. There were no
visible ectoparasites or scars, apart from some minor lacerations and callouses on
the palms of the feet and hands. The cause of death appeared to have been drown-
ing; froth and mucus were observed around the mouth and nose. Puncture wounds
were not immediately apparent. However, following skinning of the body, punc-
ture wounds were observed on the right calf, left thigh, upper tail, right chest, left
chest, and back.

Potential Predation Attempt by a Monitor Lizard


On December 17, 1984, at 1725 h, a monitor lizard (approximately 1.3 m in
length) was observed in a tree with a group of proboscis monkeys (adult male, adult
female, two immatures) a few meters above it. Another tree was immediately
adjacent; these two trees were in a clearing. The monkeys were extremely agitated,
vocalizing and making open mouth threat displays at the monitor lizard. After a
few minutes, the monkeys began leaping out of the treetop into the vegetation
below. The adult male was the last to leave. He moved into the adjacent tree and
descended until level with the monitor lizard, made an open mouth display, vo-
calized, and then leapt out of the tree. At 1733 h the monitor lizard began descend-
ing. The vocalizations continued for some minutes afterwards. It is not known
whether the monkeys or the monitor lizard entered the tree first. Presumably the
monkeys did, given their observed behavior.
64 I Yeager
River Crossing Behavior
The mean river width at markers was 17.5 m (N= 99 markers), and the mean
river width a t known crossing points was 13.5 m (N = 45 crossing points). Based
on the pooled known crossing sites, proboscis monkeys crossed the river signifi-
cantly more often a t narrower points (Kolmogorov-Smirnov two-sample test, ~ ( 2 )
= 34.63, P < 0.01). Over 50% of the known crossing sites were 13 m or less in
width; only 7% of the marker sites were 13 m or less in width. Crossing sites did
not appear to vary significantly in terms of vegetation, nor did there appear to be
habitual sites, as no site was observed being used on more than three occasions.
The four groups of proboscis monkeys were each estimated to cross the river a n
average of 3.7 times per month (range 2-6). There was no significant variation
between groups in the number of times they crossed the river ( ~ ~ ( =3 )0.7, P >
0.05). There was no significant variation between months in the number of cross-
ings made by these four groups ( ~ ~ ( = 4 )2.35, P > 0.05). It should be noted,
however, that in the FB group (adult male, adult female, infant) the female did not
cross the river for over 1 month after the birth of her infant. All crossings in July
were made by the male. On two separate days, he crossed the river, vocalized to the
female, waited a few minutes, and then crossed back to the female. The other
groups in FBs band had crossed previously.
A variety of potential predation avoidance behaviors were observed in con-
junction with river crossings, but were not quantified. These included visual scan-
ning, the use of foliage as springboards across all or part of the water, several
individuals or groups crossing simultaneously (i.e., the dilution effect or safety
in numbers), swimming rapidly across and immediately moving up into the trees,
and group stragglers or solitary animals entering the water quietly (the stealth
tactic). Of those animals crossing alone (i.e., no other animals crossing within 15
min of them in the same direction), five out of six were adult males.
Groups coordinated crossings (X = 63.3%,range 16.7%-81.8%,N = 4 groups)
more often than they crossed independently (X = 36.7%,range 18.2%-83.3%,N =
4 groups). If tentative assignments are included, groups coordinated crossings a n
average of 72.6% (range 35.3%-90%, N = 4 groups) and crossed independently a n
average of 27.4% (range 10%-64.7%, N = 4 groups). The smallest group (FB) was
most likely to cross alone. This was primarily due to the male crossing the river
alone and then returning when the female did not cross. When crossing indepen-
dently, the FB group used the aforementioned stealth tactic of entering the water
quietly and swimming across rapidly.

DISCUSSION
Proboscis monkeys appear to choose their crossing sites based on river width,
with a preference for narrower sites. This preference does not appear to be based on
swimming capabilities, a s they are excellent swimmers. Energetic constraints may
play a role here, although the few extra seconds needed to swim a n additional 3 m
would probably be negated by additional travel needed to reach a narrow point in
the river. Given the infrequency of crossing and the cautious behavior exhibited
prior to crossing, it appears that their river crossing behavior has been influenced
most strongly by the potential predators they might encounter: snakes, monitor
lizards, and false gavials. With regard to the potential of these species as predators,
monitor lizards and a variety of snake species have been observed in the vegetation
at the rivers edge and swimming in the river; venomous and constrictor species of
snakes are known to be in the area. Snakes and monitor lizards can also climb
trees. The same degree of caution seen during river crossings was, however, not
Proboscis Monkey Antipredator Behavior I 65
observed in travel and choosing feeding and resting places. Though potentially
dangerous, snakes and monitor lizards may not pose a s great a threat as false
gavials. False gavials, although generally considered to be fish eaters, are known
to have preyed on a n adult male proboscis monkey [Galdikas, 19851, a n adolescent
female proboscis monkey (this report), and a long-tailed macaque [Galdikas &
Yeager, 19841. It is clear that this predator poses a definite threat to proboscis
monkeys.
Proboscis monkeys are probably most a t risk when crossing the river. Ex-
tremely small groups, such as FB, may be able to take advantage of the stealth
tactic by itself in avoiding their predators when crossing alone. As previously
mentioned, another potential means of dealing with false gavial predation may be
for several groups to cross together or in coordination, thus overwhelming the
predators feeding capacity. For groups to synchronize movement, they need to be
in association at the rivers edge. Proboscis monkey groups associate with other
groups approximately two-thirds of the time at their sleeping sites on the rivers
edge [Bennett & Sebastian, 1988; Yeager, 1989a, 19911. One potential function of
these associations may be to allow groups to synchronize their movement with
other groups during river crossings. Groups do appear to coordinate river crossings
a t least part of the time. Predation threat may play a role in the maintenance of
intergroup associations.

CONCLUSIONS
1. Proboscis monkeys cross the river at narrower parts, probably as a n anti-
predator strategy.
2. The false gavial appears to be their major predator.
3. One potential function of intergroup associations may be to coordinate river
crossings.
ACKNOWLEDGMENTS
I thank the Indonesian Institute of Sciences (L.I.P.I.), the Center for Research
and Development in Biology (L.B.N.), and the Nature Protection and Wildlife
Management Division (P.H.P.A.) for their sponsorship. Partial financial support
was provided by Regents Fellowships and Graduate Research Awards from the
University of California, Sigma Xi, Page and Weldon Yeager, and the late Juliette
Scott. Support during preparation of this manuscript was provided in part by NIH
training grant HD07303 at the University of Tennessee. Bapak and Nina Su-
laiman and Karen and Brent Sears provided valuable assistance in Jakarta. Field
assistance was ably provided by Bapak Dullah, Mulyadi, and Kusasi. This study
could not have been completed without the emotional, logistical, and field support
provided throughout by Trevor Blondal. I also thank William A. Mason, Gary
Mitchell, Dale Lott, Donald Owings, William Hamilton, Gordon Burghardt, Eliz-
abeth Bennett, Paul Andreadis, and anonymous reviewers for their helpful com-
ments and/or discussions.
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