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Association between olive colobus (Procolobus verus) Diana guenons (Cercopithecus diana) and other forest monkeys in Sierra Leone.

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American Journal of Primatology 21:129-146 (1990)
Association Between Olive Colobus (Procolobus verus),
Diana Guenons (Cercopithecus diana), and Other Forest
Monkeys in Sierra Leone
'Departmenf of AnthropoloRy, Hunter College and fhe Graduate School, CUNY, New York
and 'Department of Biology, Unwersrty of Mtami, Coral Gables, Florula
Close association between olive colobus (Procolobus uerus) and other monkeys (especially Cercopithecus species) has been observed throughout the
range of P. uerus in the forest zone of West Africa. To investigate the basis
of this association, we made new observations in Sierra Leone, concentrated a t Tiwai Island. We obtained data on the association patterns of
monkeys over a large area of the island from line-transect samples, and
studied association behavior via long-term observational sampling of habituated groups of olive colobus and Diana monkeys (C. dmna). During
transect sampling, olive colobus always were seen less than 50 m from
monkeys of other species, especially Cercopithecus. In studies of habituated groups, we found that one group of olive colobus associated closely
with a larger group of Diana monkeys for more than 3 years. Members of
the two groups were within 50 m of each other on over 80% of scan samples; the two groups shared the same range, but foraged in different parts
of the canopy and had little dietary overlap; association was maintained by
the behavior of the colobus. The olive colobus was the only Tiwai monkey
species seen less than 50 m from members of a second Dlana study group
more frequently than expected, although in this case the two species were
associated during less than 12% of samples. In both cases, we detected
month-to-month variation in association frequency. We suggest that olive
colobus has a strong tendency to associate with other monkeys a s part of
a n evolved strategy; that observed association patterns depend on the
ranging habits and group dispersion patterns of the other species in the
area; and that this strategy evolved because it reduces predation risk for
a small-bodied monkey that forages in small, dispersed groups.
Key words: interspecific association, Promlobus verus, Cereopithecus diaria, antipredator strategy
Nearly all of the best-documented instances of interspecific associatian among
primates involve association between members of the same genus, particularly
Reeeived for publication December 7, 1989; revision accepted March 6, 1990.
Address reprint reqwsts to John F Oates, Department of Anthropology, HunterCollege, 695 Park Ave.,
New York,NY 10021.Thecurrent address of George H. "hidesides is: Biology Departmeat, GTCC, P.O.
Box 309, Jarnestown, NC 27282.
1990 Wiley-Liss, Inc.
130 I Oates and Whitesides
Cercopithecus in Africa [e.g., Cords, 1987; Gautier-Hion, 19881 and Saguinus in
South America [e.g., Terborgh, 1983; Garber, 19881. Functional explanations for
such associations between species which have overlapping diets must tease apart
potential costs and benefits of association related to foraging from those related to
other factors such as predation risk; such distinctions often are difficult or impossible to make. Some cases of frequent association between members of different
genera are known, but these generally involve species with considerable dietary
overlap [e.g., Saimiri and Cebus in South America: Klein & Klein, 1973; Terborgh,
19831. Here we document and discuss patterns of association between olive colobus
monkeys (Procolobus verus) and guenons (Cercopithecus spp.) in West African forests. These associations are of interest for two main reasons: 1)they involve species
with very little dietary overlap, and 2) they suggest that association with other
species is a n essential part of the olive colobus adaptive strategy.
Over 30 years ago, Booth [1957] noted that the olive colobus often was found
feeding in close proximity to Cercopithecus monkeys; he suggested that this was a
protective adaptation on the part of the colobus:
The more mobile, inquisitive frugivorous guenons, which must move from branch to
branch frequently in search of their food, are more likely to spot a n enemy than is the
olive colobus, which can sit on a leafy bough and consume several ounces of foliage
without shifting positions at all. Moreover, the resonant warning cries of the guenons
are observably understood and acted upon by the olive colobus.
Booth, however, did not study habituated groups of monkeys, nor did he provide
detailed, quantitative statements about diets or patterns of association. Booth
suggested that dogs, humans, and crowned hawk-eagles (Stephanoaetus coronatus)
might be “enemies” to other species of forest monkey, but he did not provide any
specific evidence of predation or attempted predation on olive colobus. In this paper
we examine Booth’s ideas in the light of evidence we collected in the course of both
line-transect surveys and long-term observations of habituated monkey groups at
Tiwai Island in southern Sierra Leone. We pay special attention to a stable association which we observed between one group of olive colobus and one group of
Diana monkeys (Cercopithecus diana diana); these two groups lived in more or less
permanent association for at least 3 years.
The olive colobus is an unusual monkey in several respects. It is the smallest
of all colobine monkeys (adult males average 4.7 kg, adult females 4.2 kg) [Oates,
19881, and the most drably colored. It has the most reduced thumb of any colobine.
Infants are carried in the mother’s mouth and, at our study site at least, do not
cling to her trunk. The species has a peculiar geographical distribution pattern,
not found in any other primate; it occurs only in coastal West Africa, in the moist
forest zone from southern Sierra Leone to eastern Nigeria; it crosses two important
zoogeographical boundaries (the Dahomey Gap and the Niger River), but does not
occur east of the Cross River [Oates, 19811.
Wherever the olive colobus has been observed in the wild, it has almost always
been seen in close proximity to monkeys of other species, especially guenons. Booth
[19571 noted that in Ghana he often saw it feeding in the company of Cercopithecus
campbelli, C . mona, and C. petaurista. Rucks [19761 often saw olive colobus in
groups with C. diana, C. petaurista, and C. campbelli in the Bia National Park,
Ghana. During surveys in the Tai National Park (C6te d’Ivoire), Galat-Luong and
Galat [1978] detected olive colobus on 24 occasions; in 22 cases these monkeys were
Olive Colobus Associations I 131
in close association with other species, most frequently C . diana, C . petaurista, and
C . campbelli. At a site in Benue State, Nigeria, J.F.O. saw olive colobus travelling
in a mixed group with Cercopithecus mona and C . nictitans [Oates, 19821.
In the course of surveys in southern Sierra Leone in 1979,1980, and 1985, we
encountered olive colobus eight times; in each case we observed Cercopithecus
species within 50 m of the colobus.
Tiwai is the largest (12 km2) and northernmost (7” 33’N, 11”21’W) in a series
of partly forested islands in the Moa River. It has sandy soils and a seasonally wet
climate; annual rainfall averaged 2,708 mm in 1983-86, with most rain falling in
May-November. About 60% of the island is covered by old-growth secondary forest, in which leguminous trees are abundant. In addition to the olive colobus and
Diana monkey, other anthropoid primates inhabiting the old forest are the red
colobus (Procolobus badius), the black-and-white colobus (Colobus polykomos), the
sooty mangabey (Cercocebus atys), the spot-nosed monkey (Cercopithecus petaurista), Campbell’s monkey (Cercopithecus campbelli), and the chimpanzee (Pan
troglodytes). Some monkeys were shot by hunters on the island in years prior to
1982, but since that date Tiwai has been protected from hunting. Further details
about the site are given in Whitesides et al. [1988], Whitesides [1989], and Oates
et al. [19901.
We studied primates on Tiwai by using a set of trails cleared through the forest
undergrowth on a 400 m grid. In two areas on either side of the island (East and
West Study Areas) this 400 m grid system was subdivided by trails at 50 m intervals. Behavioral and botanical sampling were concentrated in these areas. We
collected the observations presented in this paper in two chief ways: 1) by the
transect sampling of primate populations in the old forest (this involved repeatedly
walking along a set portion of the 400 m grid system), and 2) by systematically
sampling the behavior of habituated groups of olive colobus and Diana monkeys
inhabiting the two study areas.
G.H.W. made twenty-eight 6 km transect samples between 4 October 1982 and
21 January 1984. Anthropoid primates encountered during transect samples were
scored as “clusters.” Primates were regarded as belonging to the same cluster if,
regardless of species, they were separated by no more than 50 m from any other
detected primate. Details of the technique are given in Whitesides et al. [19881.
We habituated two groups of Diana monkeys and one group of olive colobus
monkeys to tolerate our close proximity. The olive colobus group (“PF”) inhabited
the East Study Area, and shared its range with one of the Diana groups (group
“E”);habituation of these groups began in February 1983. The second Diana group
(“W”) inhabited the West Study Area, and its habituation began in November
1982. We sampled the behavior of these groups systematically while following
them from dawn to dusk for periods of 3 consecutive days. G.H.W. sampled group
W during two 3-day periods each month from March 1983 through June 1984, and
group E for one 3-day period each month from July 1983 through June 1984. J.F.O.
sampled group PF during two 3-day periods in July 1983, January 1984, and
October 1985, and for one 3-day period in June 1983, August 1983, June 1984,
February 1985, and March 1985. We simultaneously sampled olive colobus group
PF and Diana group E on January 14-16, 1984, and June 12-14, 1984.
At 20-min intervals, we scan-sampled the behavior of individuals within a
study group. Scan samples of the olive colobus group lasted 5 min; a t the end of this
132 I Oaks and Whitesides
TABLE I. Summary of Results of Monkey Sighting6 From the
Twenty-Eight6km Transect Samples Conducted Between October
1982 and January 1984 on Tiwai Island
No. of
No. of
No. in
’ in
5 i g h t i n g s consisting of more than one conspecific individual, or if only one individual,
then confirmation (usually via vocalizationl of the presence of additional conspecifics.
bSightings consisting of only one individual of a species without confirmation of additional
conspecific individuals.
‘Because the potential advantages and disadvantages of interspecific association may be
very different for lone conspecific individuals compared with yocia1 groups, we report here
only associations among social groups.
period J.F.O. noted whether, during the sample, individuals of any other anthropoid species had been detected within 50 m of any member of the olive colobus
study group. Scan samples of the Diana groups lasted 7 min, or until five individuals were sampled, whichever came first. Olive colobus feeding also was sampled
by the “frequency” or “event” method IStruhsaker, 1975; Oates, 19881. For further
details of scan sampling see Oates 119881 and Whitesides 119891.
At 2 min before and 8 min after each scan sample (i.e., at 10-min intervals)
G.H.W. noted t h e presence of any individual heterospecific anthropoids within 50
m of any individual member of a Diana study group, as well as the 50 x 50 m grid
cell occupied by members of the study group.
Transect S a m p l e s
During t h e course of 28 transect samples, 307 clusters of monkeys were observed. These clusters contained only a single observed individual or species in 230
cases; 56 clusters contained two observed species; four contained four observed
species; and one cluster contained six observed species.
Olive colobus monkeys were observed in 17 of the clusters (5.56). In each of
these 17 clusters the olive colobus were within 50 m of some member of at least one
vther species; in ten clusters one additional species was observed; in four clusters
two other species were observed; in two clusters three other species were observed;
and in one cluster five additional species were observed. During t h e transect samples, olive colobus was the only species never observed alone (Table I). Olive colobus were observed in association with some species, especially Cercopithecus sp.,
more frequently than with others (Table 11). These patterns of association differ
from expectations based on the relative frequency with which each species was
Olive Colobus Associations / 133
TABLE 11. Observed and Expected Frequencies of
Association Between Procoloblls verus and Other Monkey
Species During Transect Samples on Tiwai Island*
*Expected frequencies based on relative frequency of sighting of groups of
each species during the transect samples (see Table 1).
Chi-squared test for observed vs. expected frequency: X2 = 10.499, df =
encountered on transects, although the difference is not quite significant (chisquared one-sample test; X2 = 10.499, 0.1 2 P > 0.05, df = 5).
The olive colobus was the first species seen in only two of the 17 clusters in
which it was observed. This frequency was significantly less than expected (binomial test: P = 0.0005, N = 17; mean probability that olive colobus first species
seen = 0.4412, given the assumptions that: 1)all species were equally likely to be
the first seen, and that 2) the observed distribution of cluster sizes seen to contain
olive colobus was an accurate reflection of the true distribution of cluster sizes
containing olive colobus).
Observations of Habituated Groups
Group composition and home range size. During the 11three-day samples
on the PF group of olive colobus between June 1983 and October 1985, the group
contained an average of 8.4 individuals (range 5-10) including an average of 1.4
infants (range 0-2). The same two adult males were present throughout, but the
number of fully adult females declined from five to one during this period. Because
the samples on both Diana study groups spanned only 12 months, fewer changes in
group composition occurred than for the olive colobus study group. Both Diana
study groups contained one fully adult male and seven adult females throughout
the 12-month period reported here, although the identity of the resident adult male
changed in both study groups; differences in size between the two groups resulted
entirely from differences in younger age classes. In July 1983, Diana group E
contained 15juveniles and four infants, in addition to the adults, giving a total of
27 group members; by June 1984, three juveniles had left the group, and the four
infants had become juveniles, producing a total of 24 group members. Diana group
W contained 21 group members in July 1983, including six juveniles and seven
infants; by June 1984, the group had lost two juveniles, and the seven infants had
become juveniles, so that the group totaled 19 members. No infants were born in
either group during this 12-month period.
134 I Oates and Whitesides
PF group members were recorded in 113 cells of the 50 x 50 m trail grid (28.25
ha), during the 11three-day samples. Because some of these cells bordered the Moa
River, and consequently were not complete 50 x 50 m cells, the total land area in
which the group was seen totaled about 26 ha. During 12 three-day samples, Diana
group E entered 101 full 50 x 50 m grid cells (25.25 h a in area) and 22 of the
partial cells bordering the river (3.25 h a in area), for a total area of 28.5 ha. This
area was almost identical in both size and location to that used by the PF group of
olive colobus which frequently associated with group E. During the 24 three-day
samples collected on Diana group W, this group entered 163 cells 50 x 50 m (40.75
ha). If only the first 3-day sample from each month is considered (i.e., the same
number of samples as for group E), group W entered 149 grid cells (37.25 ha).
Association frequencies. We observed members of the olive colobus PF
group and Diana group E in close proximity to each other on most days and during
most scan samples. For instance, during 838 scans of PF group in which some olive
colobus were detected, J.F.O. observed members of group E less than 50 m from
members of PF group on 692 occasions (82.6% of the sample). Likewise, during
2,647 scans (10-min interval samples) of group E, G.H.W. observed members of PF
group within 50 m on 2,283 occasions (86.2% of samples).
Both of these observed association frequencies represent lower bounds. Scan
sample data taken on the olive colobus PF group probably underestimated the true
association frequency between that group and Diana group E for two reasons: 1)
while a sampled individual may have been greater than 50 m from any Diana group
E member, other (undetected) PF group members may have been nearer than 50 m
to a group E individual; and 2) a n undetected member of group E may have been
less than 50 m from a n olive colobus. The samples taken at 10-min intervals on
Diana group E probably also underestimated the true association frequency with
the PF group for two similar reasons: 1)the exact location of all group E members
could not be determined simultaneously, and 2) the exact location of all PF group
members frequently was not known a t the time of the sample; both these factors
would cause some degree of underestimation of association frequencies.
Diana group W did not show such close association with a particular group of
another species as did group E. However, olive colobus were seen within 50 m of
members of group W on 11.8%of 5309 samples taken at 10-min intervals. Olive
colobus was the only monkey species seen significantly more frequently in association with group W than predicted by a computer simulation taking account of
each species’ density and group spread [Whitesides, 19891. The olive colobus seen
in association with group W were judged to belong to at least two different groups.
Behavior in association. The association between the olive colobus PF
group and Diana group E apparently was maintained largely by the behavior of
the colobus. The Diana group used a varied foraging pattern-sometimes making
slow, steady, amoeboid-like progression, foraging as it travelled; sometimes foraging for several hours within a limited area, and then making relatively rapid
linear progressions from one site to another with little foraging along the way.
When the Diana group was static or foraging slowly, the olive colobus either rested
or fed, choosing a site within or close to the area over which the Diana group was
spread. When the Diana group moved to a new area, the olive colobus usually
followed, leaving their resting or feeding site as a Diana progression got under
way, and mixing themselves with the Diana group. During linear progressions by
Diana, olive colobus individuals usually were interspersed with the last one-third
of the Diana group.
Overt agonistic and affilitative interactions between the two species were seen
very rarely. In 833 hours with PF group, J.F.O. saw only one obvious agonism,
Olive Colobus Associations / 135
when a n adult female Diana with a n infant lunged toward a n approaching olive
colobus, which backed away; G.H.W. saw no agonistic interaction in over 475 hours
of observation of group E. Occasionally we saw play between juvenile olive colobus
and juvenile Dianas, but members of the two groups appeared to ignore most of
each other’s social and sexual behavior. Overt interactions between olive colobus
and other monkey species also were rare. On one occasion J.F.O. saw a solitary
male spot-nosed monkey (Cercopithecus petaurista) approach and briefly groom
one of the adult males in PF group. On another occasion one olive colobus (possibly
a juvenile) was seen to run off quickly a t the apparent approach of a n adult red
colobus (Procolobus badius).
Territorial interactions. During the 36 sample days on Diana group E,
G.H.W. observed a t least ten major territorial encounters between group E and a
Diana group occupying an area immediately to the north. Each of these encounters
occurred on a different day and they were spread over seven different 3-day sample
periods. These intergroup interactions included loud calls by the adult male of each
group, numerous agonistic vocalizations by most or all group members, and shortduration chases (usually less than 20 m) of members of one group by members of
the other group. During five of the ten Diana intergroup encounters (including five
of the seven 3-day sample periods), vocalizations were heard both from members of
the olive colobus PF group associated with Diana group E, and from other olive
colobus apparently associated with the rival Diana group. Many of the olive colobus calls were given in apparent response to calls from the opposite group of olive
colobus, resulting in bouts of countercalling. The olive colobus call typically associated with these encounters was the “laughing” call described by Hill and Booth
[19571; we heard this call only from adult males.
During the 33 sample days on olive colobus P F group, J.F.O. noted ten bouts
of loud calling from PF group adult males that were apparently elicited by Diana
territorial interactions andlor by the detection of other olive colobus in areas close
to the PF home range. (In this case a “bout” refers to calls produced by olive colobus
while they remained in a limited part of their range, usually close to the periphery,
and while interactions proceeded with other monkey groups which also remained
in approximately the same location; the longest of these bouts lasted for just under
3 hours, within which the longest separation of two laughing calls was 29 rnin.)
Two of these ten bouts were included in the ten Diana territorial encounters witnessed by G.H.W. In three of the bouts, an adult male olive colobus in PF group was
seen sitting in the middle canopy, looking intently in the direction of the opposite
group. However, we did not observe more overtly aggressive acts between olive
colobus groups.
Our assessment of the dynamics of these mixed Diana-olive colobus encounters
is that they were initiated largely by different groups of Diana monkeys moving
into proximity with one another. Such movement often brought different olive
colobus groups into proximity, resulting in adult male countercalling by the colobus. We have no direct evidence that an olive colobus group was “using” Dianas as
assistants in territorial defence, or that the outcome of a Diana intergroup encounter was influenced by the behavior of the olive colobus.
Responses to calls of other species. Loud calls by olive colobus frequently
were clumped temporally with those of one or more other monkey species. On 33
sample days, 360 olive colobus loud calls were noted, clustered in 125 sequences
(where one sequence includes individual laughing calls separated by no more than
5 min from other such calls). Of 85 sequences not apparently connected to intergroup encounters, 40 (47.1%) followed within 5 min of the call of another monkey
species; in 17 of these cases the first monkey to call was Cercopithecus campbelli,
136 i Oates and Whitesides
% Flowers (N = 21)
E %Fruit(N=7)
% Seeds (N = 31)
% Pod Exudate (N = 0 )
% Leaf Parts (N = 166)
% Others (N= 0)
% Insects (N= 0)
% Flowers (N = 415)
% Fruit (N = 528)
% Seeds (N = 171)
% Pod Exudate (N= 303)
El % Leaf Parts (N= 274)
I % Others (N = 27)
% Insects (N = 764)
Figure l.a,b.
and in 16 cases the first caller was C . diana. Only in one instance was a n olive
colobus call first in a sequence of loud calling by several monkey species.
Loud calls by Diana monkeys also were frequently associated temporally with
Olive Colobus Associations / 137
% Flowers (N = 167)
% Seeds (N= 55)
% Leaf Parts (N= 151)
% Others (N = 10)
% Insects (N= 265)
Fig. 1. A Proportion of time spent feeding on each category for the PF group of colobus (N = 225). B
Proportion of time spent feeding on each food category for Diana group W (N = 2,482). C: Proportion of time
spent feeding on each food category for Diana group E (N = 1,080).
those of other primate species. Of 234 Diana loud calls noted by G.H.W. in the East
study area, 142 (60.7%) occurred in close temporal relation to loud calls given by
other primates, most frequently other Diana monkey loud calls.
Diana monkeys frequently gave distinctive, high-pitched alarm calls in response to the alarm calls of other animals, such as squirrels, duiker antelopes, and
birds. Olive colobus also appeared to respond to the alarm calls of other species,
including Diana monkeys, by increased vigilance behavior and frequently by shifting to less conspicuous or less exposed positions. The functions of a variety of
low-amplitude olive colobus calls were not elucidated satisfactorily in this study,
and we could not recognize a distinctive alarm call produced by the olive colobus.
Nor did we detect that olive colobus and Diana monkeys had special responses to
each other’s calls, different in quality from their responses to the calls of other
Duration of association. Our own observations combined with those of other
researchers studying primate behavior on Tiwai (particularly G.L. Dasilva, A.G.
Davies, and C.M. Hill) showed that Diana group E was in existence (and using
approximately the same range) from at least February 1983 through December
1988. Throughout this period, olive colobus monkeys frequently were seen less
than 50 m from the Diana monkeys. Recognizable individual olive colobus (serving
to identify the animals as members of the PF group) were first noted (by J.F.O.)
moving with the Diana group in March 1983 and last recorded in January 1987;
before and after these dates the same individuals may have associated with the
Diana group, but our observations do not include those periods.
Diets. The diets of olive colobus and Diana monkeys on Tiwai are very different. The foods most frequently recorded in sampling the diet of olive colobus PF
138 I Oates and Whitesides
group were young leaves, seeds, and mature leaf petioles, while the most frequently sampled foods for both Diana study groups were ripe fruits, insects, and
flowers (Fig. 1). If specific food items are considered (i.e., a food species plus the
part of that species consumed), there was little overlap between the diets of olive
colobus PF group and Diana group E, although they used almost exactly the same
area of forest. The top ten items in the diet of each group are shown in Table I11
with no overlap in items between the two species. (Note that the olive colobus diet
data presented here are from scan samples, while the data in Oates [1988]are from
event sampling.)
Activity heights. Figure 2 compares the distribution, based on scan samples,
of olive colobus and Diana activities across heights in the forest canopy. On average, the olive colobus used lower heights in the canopy than either of the Diana
study groups, despite frequent travel with Diana E group. In 38.4% of scan samples
on the olive colobus PF group, the monkeys were below a n estimated height of 15
m, compared with 25.2% of samples on Diana group E, and 27.6% of samples on
Diana group W. Although 67.7% of olive colobus travel was at or above 15 m, 53.5%
of feeding was recorded below this height. The time spent by olive colobus feeding
low down in patches of thick growth probably was underestimated; often, the
monkeys were not seen clearly when foraging in this fashion, and in those cases
they were not included in scan sample records.
Diana monkeys spent most of their time in or just below the crowns of upper
canopy and emergent trees. The upper canopy of the forest in the East Study Area
was less broken than that in the west area, but the East Area had fewer very tall,
emergent trees; this difference probably accounts for the greater frequency of
group E samples between 15 and 24 m, and the greater frequency of W group
samples between 25 and over 34 m.
Seasonal variation in association. Variation in the frequency of association
between the PF group of olive colobus and Diana group E occurred among sampling periods. Diana monkeys were seen within 50 m of PF group members on less
than 80% of PF group scans during dry season samples (January 1984, FebruaryMarch 1985) and in a sample a t the end of October 1985 (late wet season) (Table
IV). In samples of Diana group E, olive colobus were detected within 50 m of the
Dianas on less than 80% of samples in January 1984 and in August and September
1983 (wet season) (Table IV).
Major seasonal changes in the diets of both olive colobus [Oates, 19881 and
Diana monkeys (Whitesides, unpublished data) occurred at Tiwai. These changes
probably contributed to variations in association frequency. For instance, during
the January 14-16,1984, sample period, when we followed olive colobus PF group
and Diana group E simultaneously, we observed PF group members spending a n
unusual amount of time close to the Moa River bank, feeding on the seeds of the
river-fringing tree Plagiosiphon emarginatus. This food item was available for only
a limited part of the year, a time when scarcity existed of some of the young-leaf
foods favoured by the olive colobus [Oates, 19881. While the olive colobus fed near
the river during this January sample, most of the Diana group foraged inland. In
this case, the attraction of the colobus to a particular food item apparently overrode
their usual attraction to the Dianas.
The frequency of association of olive colobus with Diana group W also varied
from month to month; olive colobus were seen least frequently with group W in
August 1983 and in November 1983-March 1984 (Table IV).
Association of olive colobus with other species. On the few occasions
when the olive colobus PF group was not associated with Diana group E for several
hours, they commonly associated with a group of another species rather than
Olive Colobus Associations I 139
TABLE 111. Top Ten Plant Items in the Diet of Procolobus uerus (PF Group) and
Cercopithecus dianu (Group E and G r o u p W)on Tiwai Island, Sierra Leone*
P. uerus (PF group)
(N = 211)
Terminalia ivorensis
(young leaves)
Sapium aubrevillei
(young leaves)
Acacia pennata"
(young leaves)
Sapium aubreuillei
(mature leaf petioles)
Lovoa trichilioides
(flowersiflorai buds)
(immature seeds)
Parkia bicolor
(young leaves)
Funtumia africana
(mature seeds)
Myrianthus libericus
(young leaves)
santal inoides
(young leaves)
C. diana (group E)
(N = 1080)
C. diana (group W)
(N = 2482)
10.9 Uapaca guineensis
(mature fruit)
9.5 Landolphia hirsuta"
(mature leaf petioles)
5.2 Funtumia africana
(immature pod fluid)
5.2 Funtumia africana
4.7 Dialium guinense
(mature seeds)
4.7 Millettia leonensis"
22.3 Funtumia africana
(immature pod fluid)
8.0 Uapaca guineensis
(mature fruit)
7.8 Funtumia africana
6.9 Millettia leonensis"
4.8 Landolphia kirsuta"
(mature leaf petioles)
4.4 Combretodendron
(immature seeds)
Landolphia hirsuta"
3.9 Landolphia hirsuta"
(mature fruit)
(mature fruit)
Daniellia ogea
1.4 Millettia leonensis"
(immature leaves)
Unidentified sp. liana" 1.3 Daniellia ogea
Unidentified sp. liana" 1.3 Ficus sp. 1
(mature fruit)
*Only observations obtained during scan sampling used in summary presented here. Sample sizes represent
known food items.
"Food species is liana rather than tree.
travelling alone. Other monkey species were detected within 50 m of PF group
members in 63 of 139 five-min sample periods (45.3%)in which no Diana monkeys
were detected within 50 m of the olive colobus. In these 63 samples, spot-nosed
monkeys (Cercopithecus petaurista) were the other species most frequently detected (30 samples), and black-and-white colobus (Colobus polykomos) were the
second most common associate (21 samples).
Spot-nosed monkeys typically moved in a quiet, skulking fashion in thick
growth and often were detected only by their alarm calls, which they commonly
produced if approached closely by humans. When members of olive colobus PF
group were seen in association ti.e., within 50 m) with spot-nosed monkeys, the two
species frequently appeared to be moving together in a coordinated fashion, with
each species apparently playing a similar role in maintaining the association.
Our observations in the West Study Area at Tiwai suggested that at least two
small groups of olive colobus overlapped the home range of Diana group W. One of
these groups frequently was seen in close proximity to spot-nosed monkeys; apparently, the olive colobus associated predominantly with the spot-nosed group,
but temporarily followed Diana group W on some occasions when the Dianas were
nearby (i.e., just the reverse of the situation involving the PF group of olive colobus
and Diana group E).
Our strong impression was that olive colobus on Tiwai adopted some of the
gross behavioral patterns of other species with which they routinely associated.
140 / Oates and Whitesides
% Group W (Diana; N = 10,629)
% Group E (Diana;N = 5641)
% PF group (olive colobus; N = 1148)
7% Group W (Diana; N = 10,629)
% Group E (Diana; N = 5641)
PF group (olive colobus; N = 1148)
Percentage (A) and cumulative percentage (B) of individuals sampled for each height category for each
Olive Cdobus Associations / 141
TABLE W.The Percentage of Samples and Sample Sizes by Month in Which Each
Study Group Was Observed Within 50 sn of at Least One Individual of the Indicated
Species (the Defkition of Association)*
PF group with
C. diana
June 1983
July 1983
August 1983
September 1983
October 1983
November 1983
December 1983
January 1984
March 1984
April 1984
May 1984
June 1984
February 1985
March 1985
October 1985
Group E with
P. uerus
Group W with
P. uerus
% (N)
% (N)
70 (N)
92.1 (89)
95.7 (162)"
83.6 (51)
68.8 (154Y
94.0 (83)
63.3 (71)
70.7 (75)
85.3 (143)"
82.6 (838)
93.7 (221)
77.9 (222)
79.6 (220)
94.4 (213)
83.7 (208)
89.3 (214)
70.8 (216)
81.9 (226)
98.2 (226)
82.5 (228)
83.9 (223)
98.7 (230)
86.2 (2,647)
11.8 (5,309)
*For the P F group ofProcoZobusuerus data derived from scan samples; for group E and group W of Cercopithecus
diana data derived from 10-min samples (group samples).
aIndieates samples combined from two different 3-day sampling periods during the same month.
Thus, we observed olive colobus relatively easily when they associated with Diana
monkeys, which are conspicuous and spent much of their time in the upper canopy.
We observed them with greater difficulty when they associated with the quiet,
stealthy, spot-nosed monkeys which spent much time in vine tangles and the thick
growth in canopy gaps. Galat and Galat-Luong [1985] also noted this tendency of
the olive colobus to adopt behavior patterns of species with which it is associating,
leading to its designation of "Singe Magique" by hunters in CBte d'Ivoire.
Olive Colobus at Pujehun
The short-term observations at Pujehun in 1979 and 1980 suggested that the
olive colobus there shared a large part of their range with one group of spot-nosed
monkeys and one group of Campbell's monkeys. J.F.O. observed olive colobus
associating with these groups for several hours, switching from one group to the
other on occasions when the two Cercopithecus groups came together and then
diverged. The olive colobus apparently were not moving permanently with either
group; however, our observations were very limited in duration and therefore we
do not have records of the long-term patterns behavior of these monkeys. On one
occasion at Pujehun a n adult Campbell's monkey was seen grooming an adult olive
Potential advantages for species involved in interspecific associations usually
fall within two broad categories: foraging advantages and predator avoidance [Whitesides, 19891.The proposed foraging advantages include: 1) reduction of duplication
of effort and regulation of return time to resources, 2) increased detection of re-
142 I Oates and Whitesides
sources, 3) availability of food items otherwise unavailable, 4)increased prey capture rate, and 5) increased intraspecific competitive ability. Postulated predator
avoidance advantages include: 1) increased detection of predators, 2) increased
predator confusion, 3 ) decreased probability of discovery or capture by predators,
and 4)increased defense against predators. Potential benefits also could arise from
a combination of foraging and predator avoidance advantages (e.g., a decrease in
necessary vigilance behavior provided by association, thus allowing greater foraging efficiency). For detailed references to the above hypotheses, see Whitesides
Our observations confirm that olive colobus have a very strong tendency to
associate closely with other monkey species, especially arboreal guenons. Whitesides [1989] found that olive colobus was the only species which associated with the
two study groups of Diana monkeys more frequently than expected by chance.
We suggest that the chief benefit that olive colobus derive from associating
with these other species is a reduction in the risk of predation. Due to the lack of
dietary overlap between olive colobus and Diana monkeys (and almost certainly
the other arboreal guenons as well), most of the proposed foraging-advantage hypotheses can be rejected; those hypotheses requiring substantial dietary overlap
between species to be effective include: 1)reduction of duplication of effort and
regulation of return time, 2) increased detection of resources, and 3 ) availability of
food items otherwise unavailable. In addition, the proposed advantage of increased
prey capture rate can be rejected, because we never observed olive colobus foraging
for or eating insects [Oates, 19881. Only the final foraging advantage (increased
intraspecific competitive ability) cannot be easily rejected; however, due to the
ecology and behavior of olive colobus, we also judged this hypothesis highly unlikely.
All or nearly all of the proposed predator avoidance advantages appear highly
plausible. Olive colobus are small-bodied monkeys that typically live in small (less
than ten individuals) social groups which tend to become relatively highly dispersed during foraging. Such dispersion probably is related to the dispersion of
young leaves in the liana tangles and gaps in which the species frequently forages
[Oates, 19881. For small-bodied animals living in small groups and foraging in
thick growth, obvious advantages exist in associating with the larger social groups
of species with which they have virtually no dietary overlap, such as the Diana
monkeys on Tiwai. Factors additional to a lack of dietary overlap may influence
the choice by olive colobus of guenons a s species with which to associate in reducing predation risk. We noticed that a human observer may approach West African
colobus monkeys without detection more easily than guenons. Although we do not
know the reason for this, one contributing factor might be differences in the
evolved functions of visual and neural systems as they relate to foraging behavior
(for instance, insects are important in guenon diets).
The tendency of olive colobus to associate with other species often results in a n
association of several hours in duration (as we witnessed in the West Study Area
at Tiwai and at Pujehun, and as the observations of Galat & Galat-Luong [19851 in
Tai suggest). However, our observations in the East Study Area a t Tiwai demonstrate that the association can be a more or less permanent phenomenon. The
pattern and duration of association adopted by a particular olive colobus group
probably depend on the ranging and foraging patterns of other monkey groups
using the same area, and on local patterns of food availability.
For instance, Galat and Galat-Luong [19851reported home ranges of 29 and 33
h a for groups of six and seven olive colobus monkeys in the Tai forest, very similar
to the 26 h a used by PF group on Tiwai. But while Diana group E used a range of
Olive Colobus Associations / 143
28.5 ha, a Diana group in the Tai study area had a home range of 93 ha [Galat &
Galat-Luong, 19851. Similarly, Diana group W a t Tiwai had a larger range size
(40.75 ha) than group E, and had only temporary associations with olive colobus.
We argue that, if olive colobus have a choice of other-species groups with which to
associate, the best choice is a group of guenons with a home-range similar in size
to that needed to provide a year-round food supply for the olive colobus. If the group
of guenons has a foraging pattern compatible with olive colobus needs, then a more
or less permanent association may result. Such association would give the added
advantage of producing familiarity with the subtleties of the other species’ behaviors, especially its reaction to predators. Furthermore, the long-term nature of the
association would probably be reinforced by the learning experiences of young
Olive colobus may associate more frequently with Diana monkeys than other
guenons at Tiwai not only because of a similarity in ranging needs, but also
because of the relatively large area over which a Diana monkey group is dispersed
while foraging. Members of a single social group of Diana monkeys typically are
spread over an area greater than 100 m in diameter, while at times exceeding 200
m in diameter [Whitesides, 19891; members of other social groups of guenons
rarely were spread over a n area greater than 50 m in diameter with 20 to 30 m
being the more typical group spread (J.F.O., G.H.W., personal observation; R.
Kluberdanz, G. Davies, G. DaSilva, S. Green, and L. White, personal
communications). Such large group spreads of Diana monkeys have two potential
advantages for the olive colobus: 1) a larger array of potential feeding sites
covered by the protective “umbrella” of a guenon group, and 2) a more
far-reaching early warning system against predators, even when feeding is not in
We found interactions between olive colobus and other monkeys (at least Diana monkeys) to be essentially one-way. The olive colobus orient positively to the
other species, and are largely ignored in return. The guenons seem to suffer little
or no detriment from being followed by the colobus, and possibly gain some benefit
from the presence of extra animals that can provide warning of potential predators.
A species such as the Diana monkey, which uses a different part of the forest
canopy and has a very different diet than the olive colobus, has the greatest likelihood of receiving such benefits. Without incurring costs from increased feeding
competition, Diana monkeys may obtain warnings about predators from a layer of
the forest which they are not able to monitor closely themselves.
The tendency of olive colobus to associate with other monkeys may be part of
a genetically based evolved strategy. The behavior has been seen in all observed
populations of olive colobus, even those (such as in eastern Nigeria) that have had
no recent contact (either behavioral or genetic) with other populations. Other
components of such a n evolved strategy probably include the species’ drab coloration, low vocalization rate, and habit of spending much time inactive in thick
growth. A small group of such animals is very difficult to detect within a larger
group of noisier, more active, more colorful guenons as demonstrated by our data
from the transect surveys on the sequence of detection of olive colobus within a n
What predators might olive colobus avoid by this behavior? Struhsaker [19811
has argued that crowned hawk-eagles (Stephanoaetus coronatus) are a major factor
producing interspecific association in African forest monkeys generally. The olive
colobus, however, due to its tendency to feed in thick, tangled, low growth, probably is less susceptible to attack by crowned hawk-eagles than are most African
forest monkeys. Although smaller forest raptors might pose a threat to young olive
144 / Oates and Whitesides
colobus monkeys, perhaps mammalian and not avian predation has been the major
selective force in producing the olive colobus strategy.
Among potential mammalian predators on olive colobus are chimpanzees and
leopards, as well as humans. Until very recent times, most olive colobus populations probably shared their habitat with chimpanzees and leopards (and the immediate ancestor of the olive colobus very probably was sympatric with ancestral
forms of these larger mammals). Chimpanzees inhabit Tiwai, and suggestive evidence indicates that leopards also may be present. Chimpanzees, leopards, and
olive colobus co-occur in the Tai National Park in CGte d’Ivoire, where the forest
ecosystem is similar to that at Tiwai.
In Tai, Hoppe-Dominik [19841 studied the predation patterns of both chimpanzees and leopards. In a sample of 215 leopard scats from Tai, the olive colobus was
the only one of seven Tai monkey species whose hair was not specifically identified.
In their study of the hunting behavior of Tai chimpanzees, Boesch and Boesch
[19891 noted that groups of chimpanzees searched intentionally for middle-sized
mammals, especially red colobus. The red colobus (Procolobus badius), a close
phylogenetic relative of the olive colobus, apparently is a major prey species for
chimpanzees in more than one part of Africa [e.g., Gombe, Tanzania: Busse, 1977;
Mahale Mountains, Tanzania: Takahata et al., 19841. Boesch and Boesch [1989]
recorded two attempts by chimpanzees to hunt olive colobus in Tai, during a 7-year
period (both attempts were successful) compared with 110 attempts on (and 63
captures of) red colobus; a t Tai the population density of red colobus was estimated
at about 14 times as great as that of olive colobus [Galat & Galat-Luong, 19851.
Boesch and Boesch [1989] recorded very few attempts by chimpanzees to hunt
Cercopithecus monkeys, noting that C . diana in particular “are very agile and
much quicker than the colobus; they are hunted only when very low in the canopy.”
Tai chimpanzees search for prey while moving on the ground, but will climb into
the canopy to catch their victims. We suggest that the olive colobus (similar in
many ways to the red colobus, but with half the body size, living in smaller groups,
and feeding nearer the ground) would face a high risk of predation from chimpanzees unless they adopted a special counterstrategy.
The evidence from Tai of low predation levels on olive colobus suggests that the
species has a relatively effective anti-predator strategy. Although this evidence
(along with other evidence we have presented) does not prove that association
behavior evolved primarily in response to predation pressure, it is at least consistent with this hypothesis. Clearly, primate interspecific association behavior is
unlikely to have a single cause across (or even within) taxa, but in this case
association as part of a strategy to lower predation risk seems the most plausible
explanation of current evidence.
1. Observations in the rain-forest zone of Sierra Leone confirmed that olive
colobus monkeys have a strong tendency to associate with monkeys of other species, especially members of the genus Cercopithecus.
2. One olive colobus group a t Tiwai Island associated closely with a group of
Cercopithecus diana for more than 3 years. We studied this association and found
that it was maintained by the behavior of the colobus, which largely were ignored
by the Diana monkeys. The two species shared the same home range, but concentrated their feeding in different parts of the forest canopy and had little dietary
overlap. However, some associations between olive colobus and groups of other
species were more temporary (on the order of several hours).
Olive Colobus Associations / 145
3. We argue that the particular species with which an olive colobus group
associates in any given area, and the duration of this association, are related to the
ranging and feeding patterns of other species in that area, to patterns of food
availability, and to the distances in the forest canopy over which foraging groups
of other species are spread.
4. The olive colobus potentially is very vulnerable to predators because it is a
relatively small-bodied monkey that forages in small, dispersed groups. We suggest that the association behavior of the olive colobus is part of a strategy that has
evolved because it reduces predation risks. One potentially dangerous predator of
olive colobus is the chimpanzee.
This work was funded by grants from the National Science Foundation (BNS
8120206, 8505702 to J.F. Oates and S.M. Green), the Research Foundation of
CUNY, and the New York Zoological Society. For their help in Sierra Leone we are
very grateful to: the people of Barri and Koya Chiefdoms (especially Chiefs V.K.
Magona and M.M. Kanneh, the people of Kambama and Mapuma, and Dr. S.S.
Magona), the staff of Njala University College (in particular Mr. G. Goba, Dr. A.
Sesay, and Dr. P.T. White), personnel of the Forestry Division (Freetown), the Rev.
Pat Palmer (Pujehun), and Nigel and Rachel Wakeham (Freetown). We thank
Marilyn Norconk for inviting us to participate in the symposium at the IPS Congress in Brasilia at which an early version of this paper was presented. We also
thank three anonymous reviewers for their critical comments on earlier versions of
the manuscript.
Boesch, C.; Boesch, H. Hunting behavior of Garber, P.A. Diet, foraging patterns, and resource defense in a mixed species troop of
wild chimpanzees in the Tai National
Saguinus mystax and Saguinus fuscicollis
Booth, A.H. Observations on the natural his- Gautier-Hion, A. Polyspecific associations
among forest guenons: ecological, betory of the olive colobus monkey, Procolohavioural and evolutionary aspects. PD.
bus uerus (van Beneden). PROCEEDINGS
LONDON 129:421-430,1957.
Busse, C. Chimpanzee predation as a possiF. Bourliere, J.-P. Gautier, J. Kingdon, eds.
ble factor in the evolution of red colobus
Cambridge, Cambridge University Press,
monkey social organization. EVOLUTION
31:907-911, 1977.
Cords, M. Mixed-species association of Cer- Hill, W.C.O.; Booth, A.H. Voice and larnyx
in African and Asian Colobidae. JOURcopithecus monkeys in the Kakamega ForNAL OF THE BOMBAY NATURAL HISest, Kenya. UNIVERSITY OF CALIFORTORY SOCIETY 54:309-321,1957.
Hoppe-Dominik, B. l h d e du spectre des
1-109, 1987.
proies de la panthhre, Panthera pardus,
Galat, G.; Galat-Luong, A. La communaute
dans le Parc National de Tai en CBte d'de primates diurnes de la forGt de Tai, CBte
Ivoire. MAMMALIA 48:477-487, 1984.
Klein, L.L.; Klein, D.J. Observations on two
VIE) 40~3-32,1985.
types of Neotropical primate intertaxa asGalat-Luong, A.; Galat, G. ABONDANCE
COTE DIVOIRE. Adiopodoume, CBte d'- Oates, J.F. Mapping the distribution of West
African rain-forest monkeys: issues, methIvoire, 1978.
146 I Oates and Whitesides
ods, and preliminary results. ANNALS OF
Oates, J.F. In search of rare forest primates
in Nigerai. ORYX 16:431-436, 1982.
Oates, J.F. The diet of the olive colobus monkey, Procolobus uerus, in Sierra Leone. INTERNATIONAL JOURNAL OF PRIMATOLOGY 9:457-478, 1988.
Oates, J.F.; Whitesides, G.H.; Davies, A.G.;
Waterman, P.G.; Green, S.M.; Dasilva,
G.L.; Mole, S. Determinants of variation in
tropical forest primate biomass: new evidence from West Africa. ECOLOGY (in
press), 1990.
Game and Wildlife, Accra, Ghana, 1976.
Struhsaker, T.T. THE RED COLOBUS
MONKEY. Chicago, University of Chicago
Press, 1975.
Struhsaker, T.T. Polyspecifie associations
among tropical rain-forest primates.
Takahata, Y.; Hasegawa, T.; Nishida, T.
Chimpanzee predation in the Mahale
Mountains from August 1979 to May 1982.
ECOLOGY. Princeton, Princeton University Press, 1983.
Whitesides, G.H. Interspecific associations
of Diana monkeys, Cercopithecus diana, in
Sierra Leone, West Africa: biological significance or chance? ANIMAL BEHAVIOUR 37:760-776,1989.
Whitesides, G.H.; Oates, J.F.; Green, S.M.;
Kluberdanz, R.P. Estimating primate densities from transects in a West African rain
forest: a comparison of techniques. JOURNAL OF ANIMAL ECOLOGY 57:345367, 1988.
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