AMER. ZOOL.,
14:177-184
(1974).
Correlates of Ranging Behavior in a Group of Red
Colobus Monkeys (Colobus badius tephrosceles)
THOMAS T. STRUHSAKER
New York Zoological Society, Nezu York, New York.
and
Rockefeller University, New York, New York
SYNOPSIS. Data are presented from 17 months of systematic sampling of the food habits,
ranging patterns and distribution of food of a group of red colobus monkeys. No positive or negative correlations were found between the diversity of ranging patterns and
the diversity of diet, distribution of food species, or percentage of young growth in the
diet. There was, however, a significant correlation between the diversity of ranging
pattern and the number of days per monthly sample that the group was proximal to
or had aggressive encounters with another group of red colobus monkeys.
INTRODUCTION
Early hypotheses attempting to relate
ecology and social organization among
primates proved inadequate primarily because there was a paucity of information
on rain-forest species at the time these
hypotheses were proposed (Crook and
Gartlan, 1966). Even more recent reviews
prove inadequate as more data on rainI am grateful for the invaluable assistance given
in the identification of plant specimens to Mr. A. B.
Katende of the Makerere University of Kampala
Herbarium and to Dr. Alan Hamilton, previously
with the Department of Botany, Makerere University of Kampala. Dr. Hamilton also assisted me with
the majority of the tree enumerations. To both of
them I give my thanks. Professor Peter Marler, Dr.
Tim Clutton-Brock, Messrs. J. F. Oates, Steven
Green, Peter Waser and Mrs. Mary Sue Waser all
provided valuable discussion on the subject of this
paper, which has been to its advantage. I am grateful to Mr. M. L. S. B. Rukuba, Chief Conservator of
Forests, Uganda Forest Department for his permission to study in the Kibale Forest. Mr. A. M. StuartSmith, Uganda Forest Department, is thanked for
the loan of the Blume-Leiss Optical Height Finder.
The kind and helpful assistance of the Uganda Forest Department staff at Fort Portal and the Kanyawara Forestry Station is gratefully acknowledged. I
thank the National Research Council of Uganda for
permission to conduct my studies in Uganda. The
American Society of Zoologists kindly provided financial assistance permitting me to read this paper
at the 1972 AAAS meetings. The study was financed
by U.S. National Science Foundation grant GB
15147.
forest primates become available (Struhsaker, 1969; Crook, 1970; Eisenberg et al.,
1972).
This paper considers some of the ecological and behavioral factors affecting
ranging behavior in one group of red
colobus monkeys, a rain-forest species.
These results are part of a more detailed
report on the behavior and ecology of this
species, which is currently in preparation.
There is good reason to believe that
ranging behavior and certain aspects of
social behavior and social organization may
be closely correlated among primates. It
is plausible, for example, that the dispersion of food resources may affect ranging
patterns and thereby affect group size or
intragroup social organization. Eisenberg
et al. (1972) suggest two forms of social
organization as adaptations to exploitation of certain kinds of fruit resources: 1
(i) small, cohesive uni-male groups and
(ii) large groups that split up into small
foraging parties which spread out and then
announce the location of food trees. Expressed in another way, one might predict
that widely dispersed and clumped food
sources may necessitate a wide search pattern. Likewise a species with a predilection
for a very diverse diet may also require a
1
1 presume they mean food species whose individuals occur in widely spaced clumps or as widely
spaced individuals.
177
178
THOMAS T. STRUHSAKER
wide search pattern while foraging for
food. A wide search pattern could be accomplished in a variety of ways, including
large foraging social groups, small social
groups that have a wide intragroup dispersion but have some behavioral means
of maintaining cohesion, or small and cohesive social groups that have very wide
daily ranging patterns.
An approach to understanding this relationship begins by asking: does the distribution of food or the diversity of diet
affect the daily ranging pattern of monkey
groups? One way of considering these
questions is to compare the diet, distribution of food, and ranging patterns on a
monthly basis for a particular group of red
colobus. In other words, does the monthly
ranging pattern of a group of monkeys
vary with its diet and food distribution?
STUDY AREA AND RESUME OF
SOCIAL ORGANIZATION
ship. Three particular adult males have
remained in the group throughout this period, with no other adult males joining or
leaving. Their number was increased to
four in January 1972 when a subadult
male reached sexual maturity in his behavior and became almost physically mature. The number of adult females has
declined from eight to six during this
period. Intergroup relations are typically
aggressive, but not territorial because areas
are neither defended nor used to the exclusion of other groups. Adult and subadult males are the predominant participants and the only aggressors in these
intergroup conflicts. The usual outcome is
for one group to supplant another group,
with an apparent dominance hierarchy existing between specific groups. The home
range of the CW group is overlapped considerably, if not completely, by the home
ranges of two other red colobus groups.
METHODS AND DEFINITIONS
Data presented in this paper were collected from red colobus monkeys (Colobus
badius tephrosceles Elliot 1907) living in
the Kibale Forest of Western Uganda.
Specifically, they are from the CW group
(my main study group) which lives in compartment 30 near the Kanyawara Forestry Station (0°34'N, 30°21'E, elevation
1,524 m). This part of the forest has been
classified as a Parinari forest and is typified as being transitional between tropical
lowland and montane rain forest (Kingston, 1967). The red colobus of the Kibale
Forest typically live in heterosexual social
groups averaging about 50 in number.
There are several adult males in each
group, although they are numerically exceeded by adult females. The CW group
was smaller than average groups of red
colobus in the Kibale Forest and usually
numbered 20. This group has been under
observation from August 1970 to the
present. During this period it has ranged
in size from 19 to 25. Most of the change
in group size is attributable to births and
deaths of infants, with some apparent and
minor turnover in the juvenile member-
Data presented in this paper represent
the results of systematic samples made on
17 consecutive months from November
1970 through March 1972, inclusive. During the first week of each month I attempted to follow the CW group for five
consecutive days. Ideally, the group was
to be followed from sunrise to sunset on
each of these days, giving a total of at least
1U/*! hr of contact per day. In fact, this
ideal sample was achieved on only 7 of the
17 months (Table 1). However, the amount
of contact time with the CW group in
other months was considered adequate to
permit relative comparisons of all 17
monthly samples.
During each monthly sample the movements of the CW group were plotted on
maps of the study area having a scale of
1:2500. The maximum linear spread of
this group rarely exceeded 50 m, and it
was, therefore, relatively easy to encircle
an area on the map indicating the position of the group. Whenever the group
moved from one position to another the
time was indicated on the map and in this
179
RANGING BEHAVIOR OF RED COLOBUS MONKEYS
TABLE 1. Systematic monthly samples oj the CW group of red colobus monkeys.
Month
and year
November 1970
December
January 1971
February
March
April
May
June
August
September
October
November
December
January 1972
February
March
No. of complete
days (Si lH/ 2 hr)
with group
5
5
5
5
5
5
4
4
—
5
3
2
2
3
—
-
way their distribution of time in space
could be computed and plotted. The daily
range maps were analyzed by superimposing a transparent grid over them. The grid
was composed of quadrats that were equivalent to 50 m on a side or 0.25 hectares.
This quadrat size was selected because it
seemed to represent the minimal size possible considering my mapping accuracy,
which was about ± 10 m. The amount of
time the group spent in each specific quadrat was tallied for each day and all days
of each monthly sample were then summed
to give a monthly summary of their distribution of time in space. The amount of
time tallied in this way exceeds the total
amount of time the group was observed
because at some time in every monthly
sample they occupied at least two quadrats
simultaneously. A quadrat was scored if it
comprised at least 25% of the area occupied or if the group extended at least 10 m
into this quadrat at any given moment.
In an attempt to express the diversity
of the CW group's ranging pattern an
index of quadrat utilization diversity was
computed for each systematic monthly
sample. The Shannon-Wiener information
measure (Wilson and Bossert, 1971) was
used to compute this index,
N
H= — Xpi loge pi,
i= \
where H equals the amount of diversity
No. of incomplete
d a y s « lli/ 2 hr)
with group
_
_
—
—
_
—
5
—
—
4
3
_
5
5
5
No. of minutes
in contact
with group
3,640.
3,648.
3,607.
3,709.
3,748.
3,696.
2,965.
2,895.
-'= 1,900.
3,651.
2,172.
3,440.
2,954.
2,114.
2,472.
2,412.
2,307.
in the time spent in AT quadrats for a particular monthly sample and where p{ equals
the relative amount of time tallied for the
j'th quadrat [and loge£>t equals the natural
logarithm of this quantity]. For example,
if the CW group used only four quadrats
in a particular month and the amount of
time spent in each quadrat was equal
(25%), the index of quadrat utilization
diversity would be 1.39. If in another
month they also used only four quadrats,
but spent 70% of their time in one and
10% in each of the remaining three quadrats, the index of quadrat utilization diversity would be 0.94, which represents a
less diverse ranging pattern than in the
previous example.
Another expression of ranging pattern
is the average daily distance traveled by
the group during each monthly sample.
This daily travel distance was determined
for each day in which the group was followed from sunrise to sunset and was measured directly from the plots on the map.
The major disadvantages of this measure
are that it fails to weight area in relation
to time spent in it and that it can only
be measured for days in which the group
was followed for at least \U/2 hr, thereby
reducing the sample size.
In each month more than 100 feeding
observations were made of red colobus. In
the 17 months considered here the number
of monthly feeding observations ranged
l'8O
THOMAS T . STRUHSAKER
from 104 to 468. Each feeding observation
usually consisted of the identification of
the specific part eaten by the monkey. On
a few occasions it was not possible to
identify the plant species, but rather only
the part eaten. On a monthly average such
cases comprised less than 1% of the total
sample. Feeding observations were opera-
tionally distinguished from one another
by the following criteria: (i) a different
individual monkey feeding on the same
item, (ii) the same individual monkey feeding on a different item of the same food
species, (iii) the same individual monkey
feeding on a different food species, or
(iv) the same individual monkey feeding
on the same food item of the same food
species at least 1 hr after any previous
such observation. For example, if five
monkeys were feeding on young leaves of
the same tree species, this item would be
scored five times. If these same five monkeys
continued feeding on the same item for
more than 1 hr, this item would again be
scored five times after 1 hr had passed
since the previous scoring. If the same five
monkeys then began eating leaf buds of
the same tree, this item would be scored
five times regardless of the time interval
between the feeding on leaf buds and on
the young leaves of the same species. The
majority of feeding observations were made
of the CW group during the systematic
monthly samples. However, some observations were made outside of this time period
and of other red colobus groups living in
the same area. It was assumed that red
colobus living in the same area would have
similar diets regardless of their group that
the few feeding observations made of other
groups would not bias the results of the
CW group when added to them.
The index of food species diversity was
computed for each month using the same
Shannon-Wiener information measure described above for ranging patterns. In this
case pj equals the proportion of monthly
feeding observations tallied for the uh
food species. Again, a larger index reflects
a more diverse monthly diet.
The distribution of food species was
estimated on the basis of strip enumera-
tions throughout the home range of the
CW group. Foot trails which had been
previously cut along compass bearings and
provided access to all parts of the CW
group's home range were used for the strip
enumeration. The clearing of these trails
in no way affected the current density of
the trees enumerated. All trees within
2.5 m of the trail and that were 10 m or
more in height were identified. A height
of 10 m was selected because the red
colobus rarely descend below this level.
The transect sampled was 2,873 m long and
5 m wide. Excluding overlap areas that
occurred at trail junctions gave a total
sample area of 1.43 hectares. This represents about 3% to 4% of the total area
occupied by the CW group. Densities of
the various tree species were computed directly from these enumeration data and
expressed as number per hectare. Indices
of dispersion were computed for important
food species using the ratio of the variance/
mean (Greig-Smith, 1964). When this ratio
is less than one, a regular or uniform dispersion is indicated, if greater than one, a
contagious or aggregated dispersion. Computation of a variance and mean were possible because the tree enumeration data
were collected and segregated in 50 m sections along the entire 2,873 m transect.
Relative crown size was determined for
10 specimens each of 13 common tree species. Only mature specimens were considered. Two measures were made: maximum crown depth and maximum crown
diameter. A Blume-Leiss Optical Height
Finder was used to measure the maximum
and minimum height of foliage, the difference of which was the crown depth. Maximum crown diameter was determined with
a tape measure and was measured from the
approximate edge on one side of the
crown, through the trunk to the approximate edge on the other side. Precision in
both these measures was probably not very
great, but any source of error or bias was
believed to be uniform for all species. Consequently, comparison of the relative measures is valid. Ideally, one would like to
estimate the potential food producing area
of the tree, but because most trees have
181
RANGING BEHAVIOR OF RED COLOBUS MONKEYS
irregular crown shapes one cannot use
crown depth and width to compute surface
area or volume as would be the case if the
tree crowns assumed true geometrical
shapes. I use, therefore, the sum of the
maximum crown depth and maximum
crown diameter as an index of crown size,
which makes the fewest assumptions about
crown shape. Average values of crown size
were computed for each of the 13 species,
i.e., the mean crown depth plus the mean
crown width.2
An estimation of the relative food producing area provided by each of these 13
species is the product of their density and
mean crown size, which I call the cover
index.
All statistical results are based on onetailed significance tests of the Spearman
Rank Correlation Coefficient (rs) as described in Siegel (1956). The indices of the
various parameters were computed for each
of the 17 months and then ranked and
compared. Thus, N equals 17.
RESULTS
There was no significant positive correlation between the following pairs of indices: (i) food species diversity and quadrat
Colobus bad/us iephroscetes - CW group
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210
220
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2 60
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Index of food species diversity
FIG. 1. Monthly plots of indices of quadrat utilization diversity vs. food species diversity. Each point
represents the results for a specific month, e.g., F72
is February 1972. r, — 0.078.
2
It might be argued that the product of these two
means gives a better indication of crown size than
does their sum. However, it makes little difference
for this analysis because comparison of the sum of
these two means with their product for each of the
13 species gives rf — 0.98, which is highly significant
(P < 0.01), i.e., there is a positive correlation between the sums and products.
Colobus badius tephrosceles - CW group
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Index of cover for top four food species
FIG. 2. Monthly plots o£ indices of quadrat utilization diversity vs. the sum of the indices of cover for
the top four food species in each month; abbreviations as in Fig. 1. r, = 0.349.
utilization diversity (rs = 0.078; P >0.05;
Fig. 1); (ii) average indices of dispersion
for the top four food species of each
month 3 and quadrat utilization diversity
(rs = 0.129; P >0.05); (iii) the combined
indices of cover for the top four food
species 4 of each month and quadrat utilization diversity (rs = 0.349; P >0.05; Fig.
2); (iv) percentage of young growth
(flowers, buds, and young leaves) in the
monthly diet and quadrat utilization diversity (rs = 0.177; P >0.05); and (v) the
mean daily distance traveled per monthly
sample and the food species diversity
(r, = 0.209; P >0.05). Furthermore, none
of the above pairs were significantly correlated inversely.
In a final attempt to relate the available
measures of food distribution and ranging
pattern diversity, the monthly data were
plotted in a three-dimensional manner.
The average cover indices for the top four
food species in each month were plotted
along the horizontal axis of a graph and
3
Only the top four food species were considered
for each month because on a monthly average they
comprised 58.7% of the monthly diet (range 43.4%
to 78.7%).
4
When one of the top four food species is a species for which data are not available to compute a
cover index then the 5th or 6th ranking species is
used. This was the case in 9 of the 17 months, but
was not considered to bias the results, because even
in these 9 months the four species used for computing the cover index comprised, on a monthly
average, 47.1% of the diet.
182
THOMAS T. STRUHSAKER
against the average indices of dispersion
for the same food species along the vertical
axis. At each monthly intersection of these
coordinates was entered the index of quadrat utilization diversity for that particular
month. If some complicated, but predictable relationship existed between these
three indices, one might expect to find
"contours" on the graph, with the arrangement of indices of quadrat utilization diversity forming some pattern. In fact, no
such "contours" emerged and in some
cases very different indices of quadrat
utilization diversity occurred at the same
intersection on the graph.
These results are contrary to one's intuitive feeling that ranging patterns are
related to and vary with food distribution.
However, even if such a relationship exists,
the nature of it is not readily predictable
even on an intuitive basis. A simple correlation between dispersion, density, or
cover indices of food species and the ranging pattern of red colobus groups may not
exist, because similar ranging patterns
might result from very different trophic
reasons. For example, restricted ranging
patterns could result either from: (i) feeding on a rare species with a clumped distribution, but having a high density of food
per tree, and (ii) feeding on a common and
widely dispersed species also having a high
density of food per tree.
Furthermore, the analysis in this paper
fails to consider an important variable,
namely, the degree of phenological synchrony among the food species. For example, if the animals are feeding on a
common and widespread food species, they
will not move far if only a few trees are
bearing food in a restricted area, i.e., if it
is an asynchronous food species. Similar
complexities can also be expected when
they feed heavily on a rare and widely
spaced food species that lacks phenological
synchrony.
However, if one accepts the available
results as reflecting the actual relation between food distribution and ranging patterns, it appears that the least diverse
ranging pattern provides adequate food
for the red colobus monkeys, at least on a
short-term monthly basis. Any monthly
ranging pattern more diverse than this is
apparently in response to other variables.
One of the most likely variables affecting
ranging patterns is intergroup conflict. As
mentioned in the resumi of social organization, there is nearly complete overlap in
the home range of the CW group and two
other groups of red colobus. In addition,
at least two other groups of red colobus
infrequently enter the CW group's home
range. The aggressive nature of intergroup
conflicts, including chasing and counterchasing and the usual supplantation of one
group by the other, has obvious effects on
the movements of the groups involved in
these encounters.
There is, in fact, a positive correlation
between the number of days per total days
in the monthly sample on which the study
group had intergroup conflicts and the
index of quadrat utilization diversity
(r, = 0.520; 0.05> P >0.01; Fig. 3). There
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FIG. 3. Monthly plots of indices of quadrat utilization diversity vs. the number of days on which the
CW group had conflicts with other red colobus
groups per total number of days in the monthly
sample, r, — 0.520.
is also a positive correlation between the
number of days per monthly sample on
which the CW group was proximal
(within 50 m) to another red colobus group
and the index of quadrat utilization diversity (rs = 0.564; P «=> 0.01; Fig. 4). In
other words, in those months when the
CW group interacted more frequently with
RANGING BEHAVIOR OF RED COLOBUS MONKEYS
Colobus bad/us lephrosceles - CW group
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FIG. 4. Monthly plots of indices of quadrat utilization diversity vs. the number of days on which the
CW group was proximal (within 50 m) to another
red colobus group per total number of days in the
monthly sample, r, — 0.564.
other groups they had a more diverse ranging pattern.5
CONCLUSIONS AND DISCUSSION
The distribution of food as measured
and evaluated in this study does not allow
prediction of the ranging pattern, measured either as the diversity of quadrat
utilization or as the mean daily travel
5
Because some monthly samples were comprised
of incomplete days, it might be argued that this
would reduce the chance of observing intergroup
conflict or proximity for those samples (Table 1).
However, incomplete days in the monthly sample
were those days on which the observer left the
group for 3 to 4 hr from about 1200 to 1500 or 1600
hr. At this time the monkeys are relatively inactive
and it is unlikely that this break affected the results
on intergroup conflicts, as evaluated in this analysis.
Furthermore, of the 53 complete days of this 17month sample the CW group was proximal to another group on 34 days. On 73.4% of these days they
were first proximal to the foreign group before 1200
hr. On only 8.8% of these 34 days were they first
proximal to a foreign group between 1200 and 1500
hr. This supports the impression that those samples
on incomplete days did not unduly bias the results
against intergroup encounters. As a final check
against this possible source of bias, a Spearman
Rank Correlation Coefficient was computed for a
comparison of (i) the number of days the CW group
was proximal to another group per number of minutes I was with the CW group in each monthly sample, and (ii) the indices of quadrat utilization diversity for each month. These two measures are
positively correlated (r, = 0.451; 0.05 > P > 0.01).
183
distance. Clutton-Brock (1972) in another
study of ranging behavior among red colobus presents data supporting some of these
conclusions. For example, in his Figure
53 are data correlating the percentage of
shoots, flowers, and fruit (corresponding to
my category of young growth) and the
number of quadrats (corresponding to my
index of quadrat utilization diversity) used
by his group of red colobus. I computed a
Spearman Rank Correlation Coefficient for
these data and found that there was no
significant correlation (rs = 0.40; P >0.05).
Apparently, red colobus groups move in
a more diverse manner than is necessary
for sufficient food. However, this conclusion cannot be accepted unequivocally
because two variables of possible importance have not been considered. Neither
the degree of phenological synchrony
among the food species nor their nutritional attributes have been evaluated in a
way which allows them to be related to the
diversity of ranging pattern. As mentioned
above, similar ranging patterns could conceivably occur in different months when
the monkeys fed on asynchronous food species, which differed greatly in their pattern
of distribution. Plotting the distribution
of the nutrients essential to the red colobus
diet seems an overwhelming, if not impossible, task. The whole problem is further compounded by the possibility of
seasonal changes in the nutritional value
of a specific plant part on a particular individual tree.
In spite of the possible importance of
these variables, it is apparent that intergroup conflicts and proximity do increase
the diversity of ranging pattern among the
red colobus at Kanyawara. Given a certain
minimal monthly ranging pattern, anything more diverse than this is dependent
on the frequency of intergroup encounters,
not on food distribution as evaluated in
this study.
It is suggested as a working hypothesis
that the relatively diverse diet of red colobus monkeys permits greater independence
of their monthly ranging patterns from
food dispersion than for monkey species
with a more monotonous diet.
184
THOMAS T. STRUHSAKER
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Clutton-Biock, T. 1972. Feeding and ranging behavior of the red colobus monkey. Ph.D. Thesis.
Cambridge Univ., England.
Crook, J. H. 1970. The socio-ecology of primates,
p. 103-168. In J. H. Crook [ed.], Social behaviour
in birds and mammals. Academic Press, New York.
Crook, J. H., and J. S. Gartlan. 1966. Evolution of
primate societies. Nature (London) 210:1200-1203.
Eisenberg, J. F., N. A. Muckenhirn, and R. Rudran.
1972. The relation between ecology and social
structure in primates. Science 176:863-874.
Greig-Smith, P. 1964 Quantitative plant ecology.
2nd ed. Plenum Press, New York.
Kingston, B. 1967. Working plan for the Kibale and
Itwara Central Forest Reserves. Unpublished report for Uganda Government Forest Department.
Siege], S. 1956. Nonparametric statistics for the behavioral sciences. McGraw-Hill Book Co., Inc.,
New York.
Struhsaker, T. T. 1969. Correlates of ecology and
social organization among African cercopithecines.
Folia Primatol. 11:80-118.
Wilson, E. O., and W. H. Bossert. 1971. A primer of
population biology. Sinauer Associates, Inc. Publishers, Stamford, Conn.