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Competition predation and the evolutionary significance of the cercopithecine cheek pouch The case of Cercopithecus and Lophocebus.

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Competition, Predation, and the Evolutionary
Significance of the Cercopithecine Cheek Pouch:
The Case of Cercopithecus and Lophocebus
Joanna E. Lambert*
Department of Anthropology, University of Oregon, Eugene, Oregon 97403
Kibale National Park; Uganda; frugivory; guenons; mangabeys; Miocene;
Reports of cercopithecine cheek pouch
use and functional significance are largely anecdotal, and
to date there have been no investigations into its use by
species living in closed forest habitats. Here, I report on
cheek pouch use in Cercopithecus ascanius and Lophocebus albigena in the Kibale National Park, Uganda, between July–October 1997. Two hypotheses were evaluated: this feature was selected for because of its role in 1)
increasing feeding efficiency via a reduction in potential
feeding competition, and/or 2) reducing vulnerability to
predation. Results indicate that both species were more
likely to use their cheek pouches when feeding on contestable foods and, after filling cheek pouches, retreated to
more densely vegetated (“safer”) positions for processing
food. There was no influence of age and sex on L. albigena
cheek pouch use. Subadult C. ascanius cheek-pouched less
frequently than adults, although there were no differences
between adult males and females. There was no relationship between feeding-patch size and number of plant food
items cheek-pouched in either species. However, the diameter of breast height (dbh; a measure of patch size) of
trees in which C. ascanius used their cheek pouches was
significantly larger than the dbh of trees in which they did
not. Both species were more likely to use their cheek
pouches in the presence of greater numbers of conspecifics. These data provide insight into the relationship(s)
among oral anatomy and feeding efficiency, and facilitate
understanding into the selection for this important oral
feature in stem cercopithecines. Am J Phys Anthropol 126:
183–192, 2005. © 2004 Wiley-Liss, Inc.
Cheek pouches are found in 17 mammalian families, and have evolved independently at least four
times within the order Rodentia (Murray, 1973).
This feature appears to have evolved only once
within the Primates, and it is found ubiquitously
within the subfamily Cercopithecinae (Hill, 1966).
Unlike most other mammalian cheek pouches, the
cercopithecine cheek pouch contains glandular tissue and the digestive enzyme amylase (Rahaman et
al., 1975). Moreover, this region of the cercopithecine mouth is highly innervated, with a degree
of representation in the somatosensory area of the
brain not found in any other primate taxon (Jacobsen, 1970; Jones and Bush, 1988; Manger et al.,
1995). In contrast to the scaling patterns found in
rodents (Vander Wall et al., 1998), the relationship
between body mass and cheek pouch volume among
cercopithecines is neither isometric nor consistent
among genera (Murray, 1975). Vander Wall et al.
(1998) reported an r2 of 0.91 in the relationship
between cheek-pouch surface area and body mass in
heteromyid rodents, and suggested that the volume
of cheek pouches scales in (virtually) direct proportion to body size. In contrast, the regression coefficient across all cercopithecine genera is 0.186, and
ratios of cheek-pouch area to body weight in cercopithecines range from 0.19 (Macaca spp.) to 0.4
(Theropithecus spp.) (Murray, 1975). In the case of
cercopithecines, such variation in relative size suggests adaptation beyond that which can be explained by body size alone.
Despite its being a major taxonomic indicator
(e.g., this subfamily is referred to as the “cheekpouched” primates; Fleagle, 1999), and the fact that
this region of the oral cavity is apparently of high
selective value, the biological role of the cercopithecine cheek pouch has received surprisingly little attention. Indeed, there have only been two studies of cheek pouch use in captivity (Murray 1975;
Lambert and Whitham, 2001), and one on free-ranging savanna baboons (Hayes et al., 1992). There are
no published data on the use of this feature in closed
forest habitats. Yet the cercopithecine cheek pouch
is commonly commented upon in the primate biology
*Correspondence to: Joanna E. Lambert, Department of Anthropology, University of Oregon, Eugene, OR 97403.
Received 8 January 2002; accepted 31 October 2003.
DOI 10.1002/ajpa.10440
Published online 27 July 2004 in Wiley InterScience (www.
literature, and anecdotal reports abound. For example, citing Murray (1975) and Napier and Napier
(1967), Hayes et al. (1992, p. 478) write: “The size
and frequency of use of cheek pouches within a given
species is related, in part to the amount of predator
pressure, but more overtly to conspecific competition.” Such statements are common despite a lack of
quantification regarding cheek pouch use in situations of high/low competition and high/low vulnerability to predation.
It is apparent that the cercopithecine cheek pouch
serves a basic food-storage function. This is consistent with its function in other mammals (Vander
Wall et al., 1998). Heteromyid, geomyid, and murid
rodents employ their cheek pouches primarily to
transport seeds to their scatter hordes (Long, 1976;
Walker, 1984; Ryan, 1986; Brylski and Hall, 1988;
Vander Wall et al., 1998). Duckbill platypus (Ornithorhynchus anatinus) use their cheek pouches
while foraging on aquatic fauna; their cheek pouches
have horny ridges which functionally replace the
teeth lost by juveniles—the pouches function to
store food while it is being processed (Murray, 1975;
Griffith, 1978; Walker, 1984).
Cercopithecines likewise use their cheek pouches
for food storage. In an analysis that included observations of captive cercopithecines as well as anecdotes from wild behavior, Murray (1975) reported
that cercopithecine species are remarkably consistent in their employment of cheek pouches. In all
settings, across genera, cercopithecines tend to use a
retrieve-and-retreat pattern with food, particularly
when there is abundant food in a small area (Murray, 1975). Lambert and Whitham (2001) reported
that that cheek pouches were employed most commonly by captive Papio cynocephalus during intense
feeding; 89% of cheek-pouching events were observed during times that the keeper brought out the
main meal of the day. Similarly, Hayes et al. (1992)
found that the greatest frequency of cheek pouch use
by wild Papio ursinus took place during the middle
of the day, a time that corresponded to the most
intensive feeding bouts.
Despite this evident and fundamental food-storage function, rodents, bats, and duckbill platypus
(i.e., the array of noncercopithecine mammals with
cheek pouches) differ from primates in one very important way: they are solitary foragers, while all
cercopithecines are gregarious feeders. Moreover,
some taxa (e.g., Cercopithecus, Lophocebus, and Cercocebus) form polyspecific associations and commonly live in sympatry with several primate species
(Cords, 1987a; Gautier-Hion, 1988a,b). This suggests different potentials with regard to selection,
stemming from intraspecific and interspecific competition over food resources. Rodents compete for
limiting resources, although this is typically via
scramble processes (Vander Wall et al., 1998). The
likelihood of feeding competition (especially contest)
is clearly greater in gregarious species.
Similar to most rodent species, primates are often
preyed upon by a variety of aerial and terrestrial
predators (Cheney and Wrangham, 1987; Struhsaker and Leakey, 1990; Longland and Price, 1991;
Isbell, 1994). For example, in a recent investigation
of eagle predation in Kibale National Park, Uganda,
Mitani et al. (2001) reported that a majority of
crowned hawk-eagles’ (Stephanoatus coronatus) diet
comprised primates; Cercopithecus ascanius accounted for 68% (36/53) of the primate prey.
Given their potential for feeding competition and
vulnerability to predation, commentary and assumptions regarding the biological role of cheek
pouches in cercopithecines generally fall into two
functional explanations: 1) cheek pouches were selected for because of their role in increasing feeding
efficiency via a reduction in potential feeding competition; and 2) cheek pouches were selected for because they provide an advantage in reducing vulnerability to predation.
I evaluate the support for these explanations in
this research. Specifically, I test the hypothesis that
cheek pouches can increase feeding efficiency because they allow animals to retreat from potential
feeding competitors before incurring the costs of agonism and without having to reduce feeding rates. I
predicted that cheek pouch use would be most common when feeding on contestable resources (e.g.,
fruit). In addition, I evaluate support for the hypothesis that cheek pouch use can reduce vulnerability to
predation by allowing an animal to retrieve food and
retreat to safer, less exposed areas to process that
food. I predicted that after filling cheek pouches,
animals would move in and down, away from terminal branches in the topmost canopy of trees.
I evaluate cheek pouch use in Cercopithecus ascanius (redtail monkey) and Lophocebus albigena
(grey-cheeked mangabey) in Kibale National Park,
Uganda. Cercopithecus and Lophocebus species
share several characteristics. They are identical in
their cheek pouch area to body weight ratios (0.37;
Murray, 1975) and, like most cercopithecines, exhibit a high level of dietary flexibility (Altmann,
1998; Chapman et al., 2002; Lambert, 2002a,b).
However, there are important differences in these
two genera as well. C. ascanius are small monkeys
(species average weight, 3.5 kg). They typically consume a higher percentage of insects and leaves relative to mangabeys, live in larger, unimale social
groups characterized by egalitarian female relationships, have smaller home and day ranges, and exhibit greater group dispersion while foraging (Struhsaker, 1978; Cords, 1987a,b; Sterck et al., 1997;
Lambert, 1997, 2002a, unpublished findings). L. albigena are bigger (species average weight, 8 kg),
typically consume a greater percentage of fruit, live
in smaller, multimale social groups with female
dominance hierarchies, and have much larger day
and home ranges (Waser, 1977; Melnick and Pearl,
1987; Isbell, 1991; Olupot et al., 1994; Olupot, 1998;
Lambert et al., 2004).
Group size and social configuration, population
density, and body size can influence patterns of competition and likelihood of predation (van Schaik,
1989; Sterck et al., 1997), and here I evaluate
whether socioecological differences influence dependency on cheek pouches. I expected C. ascanius to
use their cheek pouches more frequently than L.
albigena as a consequence of their larger group sizes
(which can lead to higher levels of within-group competition), their greater population density (which
can lead to higher levels of between-group competition), and their smaller body size (which can lead to
lowered success in interspecific competition with
larger species and higher levels of predation). Regardless of species-level differences in cheek pouch
use, understanding how this feature influences food
processing and its interface with feeding competition and predator avoidance will provide insights
into the adaptive array of this subfamily.
Study site
I conducted this research with the assistance of
one full-time field worker at the Kanyawara study
site of the Kibale National Park in western Uganda.
The park has an area of 766 km2 and is situated
roughly 25 km east of the Ruwenzori Mountains, at
an elevation of approximately 1,500 m (Rudran,
1978). Annual rainfall in Kibale has increased in
recent decades; the mean annual rainfall between
1903–2000 was 1,543 mm, and from 1990 –2000 it
averaged 1,734 mm, with two rainfall peaks in March–
April and September–November (Chapman and
Chapman, unpublished data). About 60% of the park
comprises primary and regenerating forest, ranging
from medium-altitude moist evergreen to mediumaltitude semideciduous forest; the remaining 40% is
occupied by grassland and swamp communities,
abandoned farms, and wetlands (Chapman and
Lambert, 2000). While both C. ascanius and L. albigena are common in the Kanyawara study area,
there are differences in their population densities:
C. ascanius ⫽ approximately 184 individuals and
11.48 groups/ km2; L. albigena ⫽ approximately 45
individuals and 2.41 groups/km2 (Chapman and
Lambert, 2000).
Behavioral observations
We observed focal animals of C. ascanius group
and L. albigena (0700 –1800 hr) between July–October, 1997. Focal animals were followed for half-hour
sampling periods, during which time we recorded
the sex and age class (adult or subadult; no data
were collected on infants) of the animal and all feeding events in which the entire process of food acquisition, processing, and ingestion could be observed
fully and without interruption. Even in an intensive
feeding bout, animals do not place food into the
mouth continuously; feeding is often interrupted for
seconds and minutes as the animal moves, forages,
and interacts with other monkeys. Thus, in order to
standardize frequency data for cheek pouch use, I
defined a feeding event as all ingestion that took
place over the course of a 60-sec interval. During
this time we recorded the food species/part being
consumed, the number of food items placed into the
cheek pouch, and the number of items swallowed
immediately (i.e., not cheek-pouched). It is difficult
to obtain detailed observations of feeding sequences
in closed canopy-dwelling species. However, as I describe elsewhere (Lambert, 1999, 2001a), recognizing cheek pouch use in forest cercopithecines is facilitated by both physical and behavioral cues, and
even the most secluded animal in the densest part of
the canopy will become visible at times.
I used a measure of patch size to evaluate contestability of plant food. While there can be considerable
variability, diameter at breast height (dbh) has been
shown to be a reliable predictor of fruit biomass and
number of fruits in a tree’s crown (Chapman et al.,
1992). Thus, I recorded dbh as a proxy for crown
(and thus patch) size of the feeding tree. This
method is not appropriate for assessing the distribution of most insect species, since only social insects would be measurable in terms of patchiness
(e.g., colony ⫽ patch). The subject animals did not
ingest social insects. Thus, in analyses of dbh and
likelihood of cheek pouching, only feeding records of
fruit, seeds, flowers, leaves, and leaf buds are included. As further measures of potential competitive
contexts, I recorded the number of conspecifics
within 10 m and the number of conspecifics within a
tree’s crown.
In order to determine whether animals use cheek
pouches to reduce potential vulnerability to predation, I recorded the exposure of the position where
the animal procured food vs. the exposure of the site
to which it moved and processed that food. To evaluate this, I used a “safety of position scale” (Fig. 1).
This scale was calculated along three axes: 1) the
tree’s position within the canopy, 2) the location of
the animal in the tree, and 3) the local forest structure. The tree’s position in the canopy was scored as
being either: under-, middle, or upper story, or an
emergent tree. The location of the animal in the tree
was scored as being either closer to the trunk than
the periphery, or closer to the periphery than the
trunk. The local forest structure was scored as the
canopy being either open (crowns discontinuous or
separated by ⬎1 m) or closed (tree crowns contiguous or within 1 m). The resulting scale thus ranged
from 1 as the safest (i.e., least exposure to visual
predators), which was an understory tree, with the
animal close to trunk in a closed canopy, to 16 as
most vulnerable (i.e., most exposure to visual predators), which was an emergent tree, with the animal
on a peripheral branch in an open canopy.
This scale is clearly biased towards interpreting
vulnerability in terms of aerial predation by visual
predators (e.g., raptors). However, this seems reasonable, given the extremely low density of leopards
Fig. 1. “Safety of position” scale. Includes both graphic represent and index of scores indicating vulnerability to aerial predators.
in Kibale, the fact that in over 30 years of research
in Kanyawara there have been no published python
predation events on primates, and the fact that eagle predation is high. For example, in a recent 37month study of crowned eagle (Stephanoaetus coronatus) predation in Kibale, all (n ⫽ 3) observed
predation events were on C. ascanius (Mitani et al.,
2001). Primates in general accounted for 82% of all
identified skeletal remains under nests; C. ascanius
was most the most commonly represented species
among skeletal specimens (40%; 36/90), and L. albigena comprised 2% of the total species in the skeletal specimens (Mitani et al., 2001).
Focal animals and individual recognition
My primary aim in this 4-month study was to
record details of ingestive behavior and oral processing. A majority of the study animals were not known
individually, which is not uncommon in studies of
cercopithecoids in a closed-canopy habitat (Struhsaker, 1980; Struhsaker and Leland, 1988; Gebo and
Chapman, 1995; Chapman and Chapman, 2000;
Treves, 1999). I should note that several animals
were known unequivocally and several with some
assurance. The L. albigena group contained 14 individuals (2 males, 8 females, and 4 subadults), and
the C. ascanius group contained 28 individuals (1
adult male, 18 adult females, and 9 subadults). Both
adult males in the L. albigena group were identifiable by the presence of a radio collar (Olupot, 1998),
and the C. ascanius group contained only one adult
male. Two adult females in the C. ascanius group
were also previously collared (Jones and Bush,
1988). Thus, all adult males in both groups and two
females in the C. ascanius group were unequivocally
recognizable. Nonetheless, since the identity of
many C. ascanius and L. albigena females is equivocal, I cannot reject the claim that the sample of
females is biased.
Failing to recognize all individuals can be problematic if data are dominated by observations of a
single animal or a particular subset of the social
group, such as those more habituated to the presence of observers (Martin and Bateson, 1993;
Treves, 1998); this may limit the generality of the
findings (Treves, 1998). A sampling bias would be
most likely if there were a subset of females more
habituated to the presence of observers than others.
In this research, we took several measures to minimize biasing the data toward more habituated animals. First, all parts of each social group were monitored by searching for and observing monkeys
throughout the group’s spread (e.g., center of group’s
mass vs. periphery) and in both densely vegetated
and more open areas. In addition, there were two
observers monitoring the group, which minimized
the likelihood of the sample excluding shyer animals. Animals were also observed at a distance of
between 20 – 60 m, which allowed for a more oblique
angle of observation of food processing through binoculars. It also meant, as in Treves (1998, 1999),
that focal animals were typically unaware of the
presence of observers, which further decreased the
likelihood of hiding behavior in less habituated animals.
In some primate species, rank and age can affect
spatial positioning in a social group, with subordinates more often found in the group’s periphery in
species that experience high predation (e.g., Papio
cynocephalus; Ron et al., 1996). If subordinates are
more likely to be found in less desirable positions
(e.g., in more exposed areas in a tree’s periphery),
then this too could introduce a bias towards subordinates. While I cannot rule this out, unlike baboons, C. ascanius female relationships are egalitarian and amicable, decreasing the likelihood of a rank
effect on spatial positioning. Female L. albigena relationships are described as egalitarian and amicable by some authors (Sterck et al., 1997), and hierarchical by others (Melnick and Pearl, 1987; Isbell,
1991). The effect of rank on L. albigena spatial positioning (and how it may influence sampling) is
Fig. 2. Total diet of Lophocebus albigena and Cercopithecus
ascanius at Kanyawara study area of Kibale National Park,
Uganda, July–October, 1997.
thus unclear. Given these caveats, a sampling bias
cannot be entirely ruled out, and the results of this
work must be viewed as preliminary.
We recorded only uninterrupted feeding events.
Data were collected during ca. 400 observational/
contact hours, which resulted in a total of 582 complete feeding records: 391 complete feeding records
were collected for L. albigena, and 191 for C. ascanius. L. albigena used cheek pouches in 195 (49.9%)
of these feeding records; C. ascanius used their
cheek pouches in 54 (28.3%) (␹2 ⫽ 24.02; df ⫽ 1; P ⬍
Fig. 3. Percentage of cheek-pouching of food categories. a:
Lophocebus albigena. b: Cercopithecus ascanius.
Cheek pouch use and dietary category
While both species consumed food from similar
dietary categories (i.e., insects, fruit, seeds, flowers,
bark, and “other” ⫽ petioles, ferns, moss, and gum/
sap), there were differences between the two species
in overall diet (Fig. 2). C. ascanius ate significantly
more insects than did L. albigena (48.7% vs. 36.4%;
␹2 ⫽ 7.67; P ⬍ 0.01) and more leaves (24.1% vs.
9.8%; ␹2 ⫽ 53.7; P ⬍ 0.01). L. albigena consumed
significantly more seeds (8.6% vs. 1%; ␹2 ⫽ 10.8; P ⫽
0.01) than did C. ascanius, and bark as well (8.9%
vs. 3.6%; ␹2 ⫽ 5.25; P ⫽ 0.02). Although items from
all food categories were occasionally cheek-pouched
(e.g., ferns, gum, bark, or leaves), both L. albigena
(␹2 ⫽ 116.12; df ⫽ 4; P ⬍ 0.01) and C. ascanius (␹2 ⫽
15.25; df ⫽ 4; P ⬍ 0.01) cheek-pouched fruit (and
seeds) more commonly than any other broad dietary
type (Fig. 3).
Frequency of cheek pouch use was determined
over 60-sec intervals. During these intervals, we
recorded the number of food items that were placed
into the cheek pouch and the number of food items
that were swallowed immediately. The average
number of cheek-pouched food items during these
60-sec intervals was significantly greater than the
average number of immediately swallowed (i.e.,
noncheek-pouched) food items. The mean number of
food items cheek-pouched by L. albigena in a feeding
event was 9.87 (SD ⫽ 7.88; range ⫽ 1–52; n ⫽ 173);
the mean number of items that were swallowed
without being cheek-pouched was 1.89 (SD ⫽ 2.14;
range ⫽ 1–20; n ⫽ 197). In C. ascanius, the mean
number of items cheek-pouched in a feeding bout
was 6.51 (SD ⫽ 5.43; range ⫽ 1–21; n ⫽ 53); the
mean number of items that were swallowed without
being cheek-pouched was 1.69 (SD ⫽ 1.80; range ⫽
1–12; n ⫽ 143). This assessment includes not only
fruit, but also other food types that were quickly
harvested in a given location. For example, when
insects were happened upon individually, focal animals quickly swallowed them immediately (n ⫽
182). However, if the animals came upon a cluster of
insects (e.g., caterpillars), they were harvested rapidly and cheek-pouched before swallowing, with the
pouches becoming visibly distended (n ⫽ 31).
albigena individuals within a tree crown when they
cheek-pouched food was 2.53 (n ⫽ 173), and 1.9 (n ⫽
172) when they did not use their cheek pouches (t ⫽
3.8; P ⬍ 0.05).
The same pattern is evident in C. ascanius: when
they cheek-pouched food, there were more individuals (mean ⫽ 2.67; n ⫽ 39) within 10 m than when
they did not cheek-pouch (mean ⫽ 1.58; n ⫽ 98) (t ⫽
3.17; P ⬍ 0.05). The average number of C. ascanius
individuals within a tree crown when they cheekpouched food was 3.06 (n ⫽ 51), and 1.78 (n ⫽ 136)
when they did not use their cheek pouches (t ⫽ 4.76;
P ⬍ 0.05).
Measure of vulnerability to predation
Fig. 4. Percentages of subadult, adult male and adult female
cheek pouch use in Lophocebus albigena and Cercopithecus ascanius.
Measures of competition: influence of age, sex,
patch size, and interindividual spacing
In L. albigena, there was no influence of age and
sex on the likelihood of cheek-pouching: adult males
(n ⫽ 123), adult females (n ⫽ 142), and subadults
(n ⫽ 79) used their cheek pouches at similar frequencies (␹2 ⫽ 4.69; df ⫽ 2; P ⫽ 0.09) (Fig. 4). C.
ascanius subadults (n ⫽ 52) used their cheek
pouches significantly less than did adults, although
there were no differences between adult males (n ⫽
42) and females (n ⫽ 96) in their frequency of usage
(␹2 ⫽ 8.67; df ⫽ 2; P ⫽ 0.01). This is likely the result
of the fact that subadult C. ascanius engaged in
higher levels of insectivory than did adult C. ascanius (56% vs. 43%), and insects were the food least
likely to be cheek-pouched.
There was no relationship between overall feeding
patch size (dbh) and the number of plant food items
cheek-pouched in either L. albigena (r2 ⫽ 0.017; P ⫽
0.1) or C. ascanius (r2 ⬍ 0.01; P ⫽ 0.5). However, the
dbh of trees in which C. ascanius used their cheek
pouches was significantly larger (average dbh ⫽
64.93 cm; SD ⫽ 33.4 cm; n ⫽ 41) than the dbh of
trees in which they did not cheek-pouch (average
dbh ⫽ 36.23 cm; SD ⫽ 223.35 cm; n ⫽ 55; two-tailed;
t ⫽ 4.96; P ⬍ 0.01). In contrast, there was no difference in likelihood of cheek-pouching by L. albigena
as a function of dbh (two-tailed; t ⫽ 0.74; P ⫽ 0.46).
The dbh of trees in which L. albigena used their
cheek pouches averaged 56.83 cm in dbh (SD ⫽
50.76 cm; n ⫽ 150). The dbh of trees in which they
did not cheek-pouch averaged 51.25 cm (SD ⫽ 52.54
cm; n ⫽ 67).
I also found that animals were significantly more
likely to use their cheek pouches when in the presence of a greater number of conspecifics. When L.
albigena did cheek-pouch food, there were more individuals (mean ⫽ 2.28; n ⫽ 155) within 10 m than
when they did not cheek-pouch (mean ⫽ 1.65; n ⫽
154) (t ⫽ 2.95; P ⬍ 0.05). The average number of L.
The safety-of-position scale ranged from 1 (safest)
to 16 (most vulnerable). In this assessment, I evaluated whether (after filling their cheek pouches) an
animal’s score on this scale increased or decreased. I
found that both species virtually never moved to
areas of greater exposure after cheek-pouching: L.
albigena ⫽ 6/306 (1.9%); C. ascanius ⫽ 2/134 (1.4%).
In over 98% of the observations, focal animals of
both species either stayed at the same location or
moved to an area of denser vegetation cover.
In 94% of those observations in which L. albigena
moved after retrieving food, they moved to an area
with less exposure. The overall mean (n ⫽ 306) start
position score for L. albigena was 9.3. The average L.
albigena score for their end position was 7.85. The
trend is the same even after breaking down by sex
and age: the mean female L. albigena start position
had a score of 9.21, and an end score of 7.85. Male L.
albigena had a mean start position of 10.0 and end
position of 8.45. Subadult L. albigena had a mean
start position score of 8.76 and end score of 7.07.
Similar to L. albigena, in 97% of those observations in which C. ascanius moved, they moved to
more densely closed parts of the canopy. The mean
(n ⫽ 134) start position for all C. ascanius was 8.75,
and the mean end position for this species was 7.16.
The average female C. ascanius start position score
was 9.8, and end position score was 8.0. Male C.
ascanius had a mean start position score of 8.07 and
end position score of 6.97. On average, subadult C.
ascanius had a start position of 7.16 and end score of
5.7. Thus, it appears that regardless of age, sex, and
species, if animals moved after filling cheek pouches,
they moved to safer positions.
In this research, I evaluate support for the hypotheses that cheek pouch use may mitigate feeding
competition and vulnerability to predation. As expected, I did find that there were species differences
in cheek pouch frequency; however, in contrast to
what I predicted, L. albigena used their cheek
pouches more than did C. ascanius. Why this was
the case may be attributed to several potential factors that warrant future testing. Most simply, it may
be due to sampling error. The facial pelage of L.
albigena is less dense than that of C. ascanius;
cheek pouch use is consequently more obvious in
mangabeys than it is in guenons. However, while
sampling bias is plausible, I believe that species
differences in cheek pouch frequency are more likely
a function of ecologically founded variables such as
diet and habitat use. For example, during the study
period, L. albigena consumed a greater proportion of
the food types that were most likely to be cheekpouched: seeds and fruit. Insects and leaves predominated the diet of C. ascanius during the months of
this work, and these were the food types that were
least likely to be cheek-pouched.
Another possible explanation for species differences is one proposed for rodents (Vander Wall et al.,
1998). Animal species with large home and day
ranges and that travel long distances between
patches may be expected to have a greater reliance
on cheek pouches. Because of its fundamental food
storage function and its role in increasing harvesting rate (when harvesting rate exceeds ingestion
rate), cheek pouches allow an animal to transport
food as it moves from one depleted patch to another,
thereby facilitating continuous food input. In Kibale,
L. albigena are indeed known to forage over wider
home and day ranges and travel from fruit patch to
fruit patch, while C. ascanius commonly feeds on
many food types in a smaller area (Waser, 1977;
Struhsaker, 1978; Olupot et al, 1994; Olupot, 1998;
Lambert, 1997, 2000a, unpublished findings). Indeed, Isbell (1991) suggested that the reliance of L.
albigena on clumped, limiting patches of food influences the nature of female relationships and the
likelihood of increased day range length. But what
do these findings suggest for the two functional hypotheses relating cheek pouch use to predation and
Arboreal primates are more vulnerable to predation when they are at forest edges, in open forest, or
on top of the canopy (Daneel, 1979; Isbell, 1994). In
this study, both L. albigena and C. ascanius exhibited a strong tendency to retreat to more densely
vegetated areas of the tree after filling cheek
pouches. Cercopithecines in particular process food
finely in the mouth, which results in relatively slow
feeding rates (Lambert, 1999); cheek pouches
thereby allow an animal to maintain a more constant input of food in circumstances when harvesting rates are higher than ingestion rates. Filling
cheek pouches quickly in exposed microhabitats
(then retreating to less exposed areas to process
food) allows animals to minimize time spent in more
vulnerable microhabitats.
Support was also found for the hypothesis that
cheek pouches may have been selected for because of
their role in increasing feeding efficiency by mitigating feeding competition. Cheek pouches were used
more commonly when feeding on fruit, and were also
used more commonly when the number of conspecifics increased in a patch. Interestingly, cheek pouch
use increased (in both species) in larger food patches
than in smaller. These results corroborate those of
Pruetz and Isbell (1999), who found that the size of
a food patch has a direct effect on the potential for
competition. In their work on Erythrocebus patas
and Cercopithecus aethiops in Kenya, these authors
found that small food sources may be used up too
quickly to result in feeding competition, since the
finder of the food essentially uses up that food before
other foragers begin exploiting the patch. In the
present study, then, cheek-pouching may be more
important in those settings where patch size is large
enough to engender competition, but not large
enough to accommodate all group members, a condition which fits the description by van Schaik
(1989) of conditions leading to within-group competition.
In some respects, support for these hypotheses is
not mutually exclusive, and teasing apart the contributions of predation and competition as selective
pressures is complicated. For example, as discussed,
both species used their cheek pouches most commonly when consuming fruit. But when cercopithecines feed on fruit, determining whether more
frequent cheek pouch use is a function of minimizing
feeding competition or predation risk is confounded:
it may well be both. Fruit is typically patchily distributed both temporally and spatially, and is therefore conducive to feeding competition (Frankie et al.,
1974; Isbell, 1991; Van Schaik et al., 1993). Moreover, fruit is often located on the terminal ends of
peripheral branches, and therefore requires that an
animal feed in open, potentially vulnerable areas.
Additionally, the same behaviors (e.g., retrieve food,
fill cheek pouches, and retreat) that reduce vulnerability to predators are used in the avoidance of
conspecific agonism. Indeed, this particular feature
fills several so-called “biological roles” (sensu Bock
and von Wahlert, 1965), as do many anatomical
features. What served as the primary selective pressure in the evolution of cheek pouch anatomy is
another issue. Can these results elucidate the context of its evolution and maintenance?
Primates and other animals experience varying
intensities and types of competition (van Schaik,
1989; Isbell, 1991; Sterck et al., 1997; Strier, 1999;
Chapman and Chapman, 2000). It is not clear in the
present case whether within-group, between-group,
interspecific, contest, or scramble competition
served as the primary selection pressure in the evolution of cheek pouches. Given their ubiquity across
the subfamily, cheek pouches are presumably a
basal adaptation, exhibited by all cercopithecines
across a variety of body sizes, social groupings, mating patterns, group sizes, and modes of feeding competition. For example, an evaluation of data from
field anecdotes and quantified work on cheek pouch
use is not suggestive of a predictable relationship
among group size, within- and between-group competition, and cheek pouch use (Table 1).
TABLE 1. Cheek pouch use and relative size, social grouping, group size, and patterns
of intraspecific competition in all cercopithecinae genera
Cercopithecinae genus
Frequency of
cheek pouch
use (1–4)1
Cheek pouch size (1)
Large ratio ⫽ 0.37
Medium ratio ⫽ 0.31
Large ratio ⫽ 0.37
Big ratio ⫽ 0.4
Social Grouping (5–7)
Variable, but typically
1 resident male
One resident male
Variable, but typically
⬎1 resident male
⬎1 resident male
Average group
size (5–7)
relationships (8)
Variable; but
usually large
Variable; but
usually large
Variable; but
usually large
Small ratio ⫽ 0.19
One resident male
Small ratio ⫽ 0.25
Variable, but typically
⬎1 resident male
Low WG
High BG
Low WG
High BG
Low WG
High BG
High WG
Low BG
High WG
Low BG
High WG
Low BG
There are too few data on cheek pouch frequency among Cercopithecinae to give absolute frequencies; this variable is thus presented
on a relative scale.
Ratio ⫽ cheek pouch area: body weight (after Murray, 1975); WG, within-group competition; BG, between-group competition (after
Sterck et al., 1997). Note lack of consistent and/or predicable relationships among socioecological variables, competition, and cheek
pouch use. References:1, this study; 2, Walker (1975); 3, Hayes et al. (1992); 4, Lambert and Whitham (2001); 5, Cords (1987a, b); 6,
Melnick and Pearl (1987); 7, Stammbach (1987); 8, Sterck et al. (1997).
Cercopithecus aethiops differs from other Cercopithecus spp. in having ⬎1 females/group, resident/nepotistic female relationships,
and high WG and High BG (Isbell, 1991; Isbell et al., 1991).
Nonetheless, several circumstantial points mitigate the centrality of predation in favor of feeding
competition. First, in this case study, the cercopithecine least likely to be preyed upon by raptors
(and chimpanzee predators, for that matter) used
cheek pouches more than the smallest anthropoid in
the forest that also happens to be the preferred
primate prey species of crowned eagles (Mitani et
al., 2001). In addition, the results presented here on
forest cercopithecines corroborate those of the only
other three studies on cheek pouch use: in a variety
of circumstances, including captivity, open habitat,
and as presented here, in closed-canopy forest, all
cercopithecines studied to date use their cheek
pouches more when in the presence of feeding competitors. Finally, cheek pouch use continues extensively even in captivity, where the threat of predation can largely be ruled out (Murray, 1975;
Lambert and Whitman, 2001). While further testing
is clearly warranted, these factors suggest that the
primary selection for the elaboration of this anatomical feature came from maximizing energy extraction in a context of feeding competition over limiting
Regardless of species-level differences, the cheek
pouch characterizes an entire subfamily, and it
clearly must have been important enough to maintain its presumably rather expensive innervation.
As discussed earlier, the incipient form of this feature probably served as a simple food storage area,
similar in function to what is observed in other
mammals. As with rodents, this almost certainly
started as a mutation that allowed animals to press
food particles against the cheek in a favorable way to
allow for an increase in harvesting rate (Long,
1976). Molecular evidence indicates a divergence of
Colobinae and Cercopithecinae at about 12 mya,
while the fossil record suggests a split sometime
between 12.5 and 10 mya (Cronin and Meikle, 1982;
Benefit, 1999). Thus, this anatomical feature may
well date to at least 10 mya (mid-Miocene). The
Miocene epoch is generally characterized by cooling
and drying climatological events, with an associated
reduction in forest cover and food resources (Andrews, 1981). The fossil record of Africa indicates
that while monkeys were rare at the outset of this
epoch and hominoids were common, throughout the
Miocene monkeys diversified, often with many monkey species occurring at the same site, while ape
richness declined. Over time there was increasingly
greater monkey biomass and species diversity competing for relatively fewer available resources.
Most explanations for the evolutionary success of
Old World monkeys (over apes) in the mid- to upperMiocene suggest that cercopithecoids adopted a
more efficient strategy in competing for increasingly
rare resources (Napier, 1970; Temerin and Cant,
1983). I argue elsewhere (Lambert, 1998, 2001b,
2002a,b) that digestive flexibility in living cercopithecines gives this subfamily a competitive edge
over ape counterparts in allowing them access to
lower-quality food resources. I suggest here that
cheek pouches may be seen as part of this competitive adaptive repertoire. Cheek pouches allow smallerbodied species to increase their feeding efficiency and
mitigate feeding competition by facilitating a retrieve-and-retreat pattern.
Cheek pouches may also facilitate access to foods
not palatable to apes. Unripe fruit is high in starch
(a storage polysaccharide) that needs to be hydrolyzed by amylolytic enzymes (e.g., amylase) before it
can be converted to simpler sugars (Lambert, 1998).
The cercopithecine cheek pouch is so high in amylase enzymes that approximately 50% of starch is
digested with 5 min of its ingestion directly at the
site of cheek pouches (Rahaman et al., 1975). It is
well-documented that extant guenons and mangabeys consume greener fruit than sympatric chim-
panzees (Wrangham et al., 1998; Conklin-Brittain et
al., 1998; Lambert, 1999, 2002b). Having the capacity to break down the starch in unripe fruit into
glucose more readily than their ape counterparts
may help to explain these patterns.
It is impossible to directly measure feeding competition in fossil species. Interpreting the biological
role(s) of soft-tissue anatomy in the fossil record is
likewise a challenge. Nevertheless, as we learned
from dental and locomotor studies (e.g., Kay, 1984;
Gebo, 1989; Garber, 1992; Fleagle, 1999; Plavcan et
al., 2001), quantifying the biological roles of anatomical features in extant animals can provide insights
into adaptations in extinct animals, and represents
a primary goal in ecomorphology. I thus suggest that
at some point during the cercopithecine radiation,
these monkeys not only increased the breadth of
their dietary niche and increased their efficiency at
using a wide diversity of foods, but as a consequence
of their cheek pouches they also become better at
harvesting foods quickly and retreating from potential feeding competitors, not only apes, but increasing numbers of monkey species as well. The evolutionary and ecological success of this, the most
speciose of primate subfamilies, may be due in large
part to their flexibility and efficiency at extracting
energy from a given habitat.
Patrick Kataramu was invaluable for his assistance in the field. Many thanks are owed to William
Olupot for allowing me to employ his radio-telemetry equipment and for discussions regarding mangabey ecology, to Paul Garber for his thoughtful feedback on the manuscript, to Frances White for
friendship and intellectual input during the final
writing phase of this paper, and to my anonymous
reviewers for their critical comments. Support for
this research was provided by Colin Chapman during my postdoctoral tenure at the Department of
Zoology, University of Florida. I thank Colin and
Lauren Chapman for facilitating all phases of this
research while in Uganda. Permission to work in the
Kibale National Park was provided by the Makerere
University Biological Field Station, the Office of the
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