Cheek pouch’s use and function: testing the Intragroup Competition versus
Predation Hypotheses
Cheek pouches, as a primitive trait of the subfamily Cercopithecinae, are one of the
few morphological specialisations linked with dietary adaptations that have been
greatly overlooked. This paper tests two functional hypotheses: the Intragroup
Competition Hypothesis (ICH), which states that cercopithecine’s cheek pouches are
used to reduce within-group contest feeding competition, and the Predation Risk
Hypothesis (PRH), which states that cheek pouches are used to increase the energy
intake in potentially risky areas allowing food to be transported away and processed at
a safe site, while minimising exposure time. This study establishes the context (i.e.
spatial distribution) for feeding competition prior to the evaluation of the ICH
hypothesis. The hypotheses were tested with data from a troop of yellow baboons,
Papio cynocephalus, (N=24) observed during a period of 12 months in Mikumi
National Park, Tanzania. Results showed that cheek pouch use was not associated
with competitive contexts of the contest type. In addition, there were no individual
differences (i.e. age, sex and rank) in cheek pouch use. Pouch use was associated with
predator risk positioning and the likelihood of a predator encounter. The findings are
supportive of the anti-predator function of cheek pouches used to assist the animal's
food acquisition, minimising time spent in hazardous sites. The study concludes that
there is no evidence indicating that cheek pouches provide a reduction of group living
costs, as there is no evidence that the use of these minimises the effects of contest
feeding competition on animals.
Keywords: contest competition, intragroup competition, predation, cheek pouches
1
INTRODUCTION
Whilst intraspecific competition is widely accepted as an important factor driving the
evolution of primate social behaviour (Alexander 1974; Kummer 1979; Dunbar 1988; Sterck
et al. 1997) and described as far more important than intergroup competition (Janson 1985),
predation is considered one of the most important selective pressures on animals (Dunbar
1988; van Schaik 1989). It is held to possess the power to modify behaviour and morphology
(Alexander 1974; van Schaik 1983, 1989; Stanford 2002).
In coping with intragroup competition costs, primates have the option of employing
different resource exploitation strategies. The ratio of costs to benefits for each strategy may
differ depending on an individual's competitive ability (i.e. sex, dominance rank and age). As
a consequence, different behavioural profiles may emerge if each individual chooses its
'optimal strategy'. Strategies that have been identified in cercopithecines include: (a)
independent foraging at greater distances from the troop centre, which has been associated
with adult males (Post 1981); (b) feeding on less valuable items to avoid food competition
(Saito 1996); (c) reducing foraging efficiency of other females by supplants (e.g. Barton &
Whiten 1993); (d) choosing a safe (central) position (van Noordwijk & van Schaik 1987; van
Schaik 1989); (e) gaining priority of access to foods and thereby increasing tolerance by the
dominant animals (Sigg & Falett 1985; Belisle & Chapais 2001) and (f) the use of cheek
pouches to reduce intragroup feeding competition costs (Murray 1975; Lindburg 1977;
Richard 1985; Deutsch and Lee 1991; Lambert and Whitham 2001; Lambert 2005). These
studies have not directly focused on pouching behaviour (but see Murray 1975; Hayes et al.
1992; Lambert and Whitham 2001; Lambert 2005), have been descriptive (Murray 1975;
Hayes et al. 1992) and mostly conducted in captivity (Murray 1975; Lambert and Whitham
2001). Field investigations are extremely rare (but see Lambert 2005) and consequently, very
little data is available in the literature.
On the other hand, in coping with predation, animal’s behavioural responses include:
the forming of large groups (Hamilton 1971; van Schaik 1983), polyspecific association
2
(Cheney & Wrangham 1987; Struhsaker 1981), vigilance (Cowlishaw 1998; Steenbeek et al.
1999; Hill & Cowlishaw 2002), spatial positioning (Hall & DeVore 1965; Rhine & Westlund
1981; van Noordwijk & van Schaik 1987; Ron et al. 1996), alarm calls (Cheney & Seyfarth
1981) and/or the selection of raised positions (Cowlishaw 1993). Some anti-predator
strategies identified are of the morphological type, and may include for example camouflage
(e.g. olive colobus monkey, Oates 1994), large incisive structure in adult males (Plavcan &
van Schaik 1992) and some authors suggest the presence of cheek pouches may allow the
animal to reduce its exposure time in predator risk environments by transporting foods to
safer positions (e.g. Richard, 1985; Caldecott 1986; Lambert 1998). Although the
implications of such use are considerable, the contention remains largely unsubstantiated.
Lambert (2005) is the only published work to date that directly evaluates cheek pouch
use as both a strategy to reduce feeding competition and to mitigate vulnerability to predation
in forest dwelling Cercopithecus ascanius and Lophocebus albigena. The study showed that
animals irrespective of sex and age filled their cheek pouches and retreated to safer sites in
order to minimise times spent in unsafe sites. Although patch size, used to estimate
contestability of food, was not associated with cheek pouch use, the use of cheek pouches in
both species increased with the number of neighbours in a patch and in C. ascanius took place
in larger fruiting trees. These findings are said to suggest that animals use their pouches to
mitigate the costs of intragroup competition. Unfortunately, the study wasn’t able to examine
the use of cheek pouches in relation to the individual’s resource holding capacity (i.e. animals
with less holding capacity are expected to use cheek pouches more than animals that can
monopolise a food resource), which may help distinguish between the two hypotheses tested
(e.g. all animals regardless of rank must minimise predation risk).
Baboons’ feeding behaviour differs from C. ascanius and L. albigena in that their diet
includes a wider range of foods that vary in relation to processing costs (Norton et al. 1987).
The greater variability in the behavioural ecology of Papio cynocephalus provides a good
opportunity to examine cheek pouch use and evaluate the hypotheses.
3
This study sets out to test two hypotheses of the use and function of cheek pouches:
(1) the Intragroup Competition Hypothesis (ICH) whereby cheek pouches are used to
maximise food intake that could otherwise be lost in competition to other associates, reducing
the effects of contest feeding competition on animals. We predicted that (a) individuals would
use their cheek pouches more (i.e. fill, distend and empty) when the risk of contest
competition is high. In an attempt to minimise inferences (i.e. test as many steps as possible in
the argument), we first established the context for contest feeding competition. We did this by
examining feeding interference rates in relation to spatial distribution of resources; and that
(b) in a multimale social group with female dominance hierarchies, differences in pouch use
will be expected with varying competitive abilities. We predicted an inverse relationship
between cheek pouch distension, filling and emptying and the ability to monopolise a
resource as measured by age, sex, and dominance rank. That is, younger individuals will use
their pouches more than older individuals, females more than males, and low-ranking animals
more than high-ranking individuals. (2) The Predation Risk Hypothesis (PRH) states that
cheek pouches are used to increase the acquisition rate in potentially risky areas, minimising
exposure time and therefore reducing the likelihood of capture. At times when animals
perceive danger, food can be easily transported and processed at safe site. We predicted that:
(c) animals would take advantage of their cheek pouches in high predator risk positions. Risk
indicators such as vegetation cover, animal height and number of neighbours in proximity will
be associated with cheek pouch filling and distension. In addition, exposed positions will be
associated with other anti-predator behaviours such as vigilance as well as cheek pouch filling
and distending when the animal is feeding. (d) Since evidence suggests that body size is not
negatively associated with predation rates (Cowlishaw 1993, 1994; Zuberbühler & Jenny
2002), this hypothesis predicts no individual differences in anti-predator behaviours. This
study assumes that all animals are equally vulnerable to predation and need to minimise risks.
However, if animals are differentially exposed to predation risk sites (e.g. low ranking
animals spending more time in unsafe positions), these differences should be reflected in the
use made of anti-predator behaviours. Therefore, when there are no differences in unsafe
4
positioning between animals: no sex, age or rank differences will be observed in outward
vigilance and cheek pouch behaviours. When differences in unsafe positioning occur: animals
that spend more time in unsafe positions will also spend more time scanning the environment
and more time filling and distending their cheek pouches. (E) As the likelihood of
encountering a predator is not constant, it is assumed that animals, in order to survive, tune
their behaviour according to their perception of danger. For example, animals are more likely
to be vigilant on days that follow a predator encounter (citation). Therefore, we predict that
pouch emptying will be associated with safe positions when the probability of a predator
encounter is high. For example, animals will transport food stored in pouches away from the
acquisition site when the probability of encountering a predator is high. Alternatively, when
the probability of an encounter is low, pouch emptying will not be associated with safe
positions with regard to predator risk, as it is energetically more costly to transport food away.
Although cheek pouches may serve multiple functions and some of these capacities
may be by-products of selective pressures for other abilities, the aim of this paper is to focus
on two of the potential current functions of this anatomical trait (see Gutierrez 2003
unpublished findings that support other functional explanations).
5
METHODS
Study Area and Subjects
This study was conducted in Mikumi National Park, Tanzania, from January 1998 to
January 1999. The data presented here come from all members of the long-term studied
Viramba Troop of Papio cynocephalus except infants (N=24). Troop history can be found in
e.g. Rhine & Westlund (1981) and Rhine (1986).. Brachystegia woodland characterises the
study area, which receives an average of 842 mm of rainfall per year. Further details
regarding habitat and ecology of the study site can be found in Norton et al. (1987).
Baboon predators in Mikumi include leopards, lions, hyenas, birds of prey and wild
dogs. With the exception of wild dogs all others are thought to be very common. Overall,
based on the number of potential predators (as well as tracks encountered), reported attacks
and alarm calls recorded, researchers are largely of the view that a high predation risk exists
for the Viramba baboons (Anderson 1986; Norton, pers. comm).
Sampling RegimeFocal animal follows were conducted from 7am to 5pm for periods
of thirty minutes (with 2-minute sample intervals) recording a total of 1,126 hours of
information. Both instantaneous and one-zero time sampling methods (Martin & Bateson
1986) were used.
Contest Feeding Competition
Despite inconsistency in how different studies have measured feeding competition of
the contest type (e.g. Janson and van Schaik 1988), the recording of the frequency of spatial
displacements in the feeding context seems to be the most frequently used and best available
measure of the intensity of feeding competition (Post 1978; Shopland 1987; van Schaik and
van Noordwijk 1988; Barton 1989; Barton and Whiten 1993; Saito 1996; Sterck and
6
Steenbeek 1997), providing valuable information about the variation in the levels of contest
competition which animals experience. Another less commonly used estimate of feeding
competition, the number of neighbours in proximity, was avoided as it is problematic (but see
Barton 1989; Hayes et al.1992; Shopland 1987). Firstly, spacing may be in itself a strategy to
reduce competition when predation risk is low (van Schaik and van Noordwijk 1988) and may
therefore not be a reliable estimate when animals have provided for anti-competition
behaviours. Secondly, when feeding on patches, animals that have contested their access to
the food patch may not be able to monopolise resources further, particularly if food is of
similar quality and abundant. These animals may then simply scramble rather than contest for
food. Thirdly, the female’s reproductive status has been shown to relate to the number of
neighbours (Barton 1989, Gutierrez 2003 unpublished data). Consorting and lactating females
were more likely to attract a higher number of neighbours. Finally, a high number of
neighbours in proximity may simply reflect the physical structure of the arboreal patch. For
the same study population, individuals feeding on ground level were found to have a higher
number of neighbours than those feeding on the crown (Gutierrez 2003 unpublished data).
The two-dimensional ground space appeared in fact more extreme in terms of clumping of
fallen foods and individuals were necessarily clumped in space. Hence, ‘feeding supplants’
were recorded to examine contest competition by food distribution. Supplants given and
received were analysed using one-zero sampling, which was preferred because it is a more
reliable estimate of rapid event-like behaviours (Hawkins 1999; Martin and Bateson 1986).
Food distribution
Food distribution was categorised into clumped and dispersed. 'Clumped distribution'
was defined in line with other studies (e.g. Shopland 1987) as a concentrated food site (i.e.
single-tree, multiple trees, shrubs or herbaceous clumps) where at least 40% of adult/sub-adult
members fed. To exclude rapid visits to food patches, a minimum visit time of ten minutes
was necessary in order to record a patch feeding event. Only one food distribution type per
7
follow contributed to the mean length of time spent per individual. Dispersed feeding was
recorded when animals foraged on non-patchy foods.
Cheek Pouch Use
Cheek pouch use was defined both as a dynamic (i.e. filling and emptying) and as a
static measure (i.e. distension), and recorded using instantaneous time sampling. Cheek pouch
filling was defined as any increment in pouch distension; pouch emptying was defined as any
chewing of foods stored in cheek pouches; and finally, pouch distension was defined as the
degree of distension of cheek pouches. In order to measure distension, pouch capacity was
divided into ‘less than one-third full’, ‘one-third to two-thirds full’ and ‘two to three-thirds
full’ and recorded on each side.
Predation Risk Three variables were used in the definition of predation risk. (1) Attacks are more
successful when baboons are in high cover where visibility is poor (Cowlishaw 1993). Cover
of the prey animal was recorded as the degree of visibility assessed at the baboon eye-level in
a three-metre perimeter. Categories used were low cover (i.e. more than two thirds of the
animal's body is visible) and high cover (i.e. one third or less of the animal's body is visible).
(2) Height of the animal's position. Lower heights are related to higher predation risk
(Cowlishaw 1993; Steenbeck et al. 1999). As tall tree heights reduce the possibility of attack
by some important predators (e.g. lions), baboons are said to be safer at heights above two
metres (Cowlishaw 1993). Height of the animal was categorised at ground level and above
two-metres (e.g. on tree crown). In order to control for rank bias, categories were allocated
with approximately the same number of low, medium and high-ranking individuals. (3)
Number of neighbours. Individuals with more neighbours are said to be in less danger (van
Noordwijk and van Schaik 1987; Steenbeek et al. 1999; Olupot and Waser 2001) because
8
more animals are vigilant and capable of detecting the predator. In addition, more animals in
proximity reduce the probability of being selected for attack. And finally, more animals can
deter predators in case of retaliation. The number of neighbours in proximity of the focal
animal was defined as the number of troop members within a three-metre radius. This was
chosen as a conservative estimate to control for the effects of within group competition
(Robinson 1981). The spatial position of the animal was recorded on every instantaneous
point sample.
Cover, height and the number of neighbours in proximity were combined to define a
safe versus unsafe position of the focal animal. A safe position was indicated by low cover,
height above 2 metres and at least two neighbours within three metres of the focal animal. An
unsafe position was indicated by high cover, ground level height and no neighbours within
three metres.
Probability of Predator Encounter
The probability of a predator encounter was defined as the likelihood of meeting a
predator based on an animal’s past predator encounters. It is the probability of coming across
a predator assuming the outcome of the previous day's encounter. This assumes that animals
will engage in anti-predator strategies all the more immediately following a predator
encounter. The effect of interacting with a predator was examined only during the day
following an encounter. This was considered a conservative approach. Two categories were
used: (a) high probability: animals experienced predator encounter on previous day; and (b)
low: animals experienced no predator encounter on previous day.
9
Vigilance
Vigilance of the animal's surroundings was recorded as an estimate of the animal's
anti-predator strategies. Although not free from confounding problems (Stanford 2002), there
is some evidence for the anti-predator function of scanning behaviours (Cowlishaw 1998;
Steenbeck et al. 1999). Outward vigilance (i.e. 'scanning the environment' where there is no
other troop member) was recorded in the form of visual scan of the animal's surroundings and
clearly distinguished from inward scanning for other troop members, which is not considered
in this study. Small juveniles were excluded from analyses as they may still rely on other
members for vigilance.
Individual variables
Animal's sex, age classes and rank categories were recorded. Age was categorised as
small juvenile (i.e. 1-2,5 years), large juvenile (i.e. 2,5-1st consort or 5 years), sub-adult males
(i.e. 5 years- transfer) and adults. Rank was categorised as high, medium and low dominance
using tertiles of dominance cardinal rank computed using Zumpe and Michael (1986).
Statistics
All sets and subsets of data tested for normality using the Kolmogorov-Smirnov test
(Sokal and Rohlf 1995) conformed to the normal distribution (P>0.05). Multivariate analysis
was used where overlap between samples made it possible (most cases). Effect sizes are
reported for significant p-values. All statistical tests are two tailed, with alpha set at 0.05.
Bonferroni post hoc tests were employed where significant effects were observed in analysis
of variance.
10
RESULTS
Food distribution and Feeding supplants
Food distribution categories differed significantly in the feeding supplant rates
observed (Paired t-test: t23=-3.126, P=0.005, d= 0.732, see Figure 1). Animals encountered
higher rates of supplants while foraging for dispersed foods than while feeding on clumped
resources. These results revealed that animals experienced greater competition while foraging
for dispersed food resources.
Cheek pouch use and food distribution (Prediction A)
Repeated measures analysis of variance examining the association of resource
distribution with cheek pouch distension, filling and emptying revealed significant differences
(F(1,23)=107.838, P<0.001, partial η2=0.82 ; F(1,23)=45.257, P<0.001, partial η2=0.66;
F(1,23)=4.731, P=0.040, partial η2=0.17, for pouch distension, filling and emptying
respectively). In particular, animals spent significantly more time distending (see Figure 2),
filling and emptying their pouches while feeding on clumped resources than while foraging
on dispersed foods.
11
Figure 1 Feeding supplant rates by food distribution: clumped feeding versus dispersed
foraging (mean/+SE). Paired t-test: t23=-3.126, P=0.005; d= 0.732.
5
Feeding supplants (%)
4
3
2
1
0
Clumped
Dispersed
Figure 2 Cheek pouch distension by food distribution (mean/+SE), F(1,23)=107.838,
P<0.001, partial η2=0.82.
Pouch distension (% of instants)
70
60
50
40
30
20
10
0
Clumped
Dispersed
12
Pouch use and competitive ability (Prediction B)
Results from multivariate analysis revealed no association between the animal's
competitive ability and cheek pouch use.
Sex: cheek pouch distension in females was not significantly different from males
(F(1,11)=0.617, P=0.449). Similarly, sexes did not differ in cheek pouch filling (F(1,11)=0.082,
P=0.780 nor cheek pouch emptying (F(1,11)=0.470, P=0.507).
Age: there was no significant main effect of age categories on baboons' cheek pouch
distension (F(2,11)=1.858, P=0.202, cheek pouch filling (F(2,11)=1.715, P=0.225), or cheek
pouch emptying (F(2,11)=0.582, P=0.575). Using a non-categorical measure (i.e. years of age)
yielded similar results (p>0.05 for all Pearson correlations).
Dominance Rank: No significant differences in cheek pouch distension (F(2,11)=0.823,
P=0.464), cheek pouch filling (F(2,11)=0.126, P=0.883) or cheek pouch emptying (F(2,11)=0.600,
P=0.566) were observed between rank categories. Results from correlation analysis using the
animal's cardinal dominance rank (i.e. percentage score in rank) and the percentage of pouch
distension, filling and emptying were consistent with multivariate analysis (all p>0.05).
It is possible that animals put into place behavioural strategies other than cheek pouch
use to deal with ‘everyday competition’, and that these being sufficient, do not require cheek
pouch exploitation. However, during resource scarcity, animals with low competitive ability
may need to invest in an additional strategy to cope with even greater levels of contest
competition. If these are the underlying mechanisms of coping with competition, rank effects
should become apparent under these severe periods. However, there is evidence that this not
the case. No rank differences in cheek pouch use were observed during the period of greatest
food scarcity1 (all p>0.05), which interestingly corresponds to the season of greatest use of
cheek pouches.
1
Patch richness was defined as amount of edible food available in a patch in relation to the total patch
capacity. Rich, medium and scarce patch richness categories were obtained combining both measures
of food quantity and food availability (Gutierrez Diego, 2003 unpublished data).
13
Predator Risk and Pouch Use (Prediction C)
Predator risk indicators were good predictors of the animal’s behaviour. Overall,
animals avoided unsafe positions, spending very little time in these. Baboons spent more than
twice the time in safe compared to unsafe locations. (Paired t test: t23=6.394, P<0.001, d=2.07;
see Fig. 3). Most of the daylight time (i.e. 80%) was spent in conditions that fell between
these two extreme safety categories. However, when animals took unsafe locations, they
distended and filled their cheek pouches significantly more than when they were in safe
positions (Paired t test: t23=12.076 P<0.001, d=3.27 and t23=6.470, P<0.001, d=1.92 for pouch
use and filling respectively, see Fig. 4). In addition, compared to safe contexts, unsafe
contexts elicited higher rates of outward vigilance (Paired t test: t23=2.217, P=0.037, d=0.55).
In order to ensure that these results were not an artefact of differences in the availability
of predator risk positions, differences in the relative availability of safe and unsafe positions
were examined by testing for the differences in the proportions of follows in which any time
was spent in either a safe or unsafe position. A test for the equality of the proportions (Arcus)
revealed no significant differences between proportions (proportion
unsafe=0.30,
proportion difference=0.045, 95% CI for proportion
safe=0.34,
difference
proportion
=0.018 to 0.081,
p=0.002). Thus, discountingdifferential availability of positions as a confounding variable.
In addition, animals used their cheek pouches to compensate for lower food intake
immediately after predator encounter. After a predator encounter, pouch use first decreased
below normal levels and then increased steadily with time (see Figure 5).
14
Figure 3 Time spent in safe versus unsafe positions by all troop members (mean/+SE).
Paired t test: t23=6.394, P<0.001, d=2.07.
16
Time spent (% of instants)
14
12
10
8
6
4
2
0
Safe
Unsafe
Figure 4. Time spent using and filling pouches by risk of place (mean/+SE). Paired t test:
t23=12.076 P<0.001, d=3.27 and t23=6.470, P<0.001, d=1.92 for pouch use and filling
respectively.
50
45
Pouch use
Pouch filling
40
Time spent %
35
30
25
20
15
10
5
0
Safe
Unsafe
15
Figure 5 Pouch distension and occurrence of predator encounters in minutes (mean/+SE).
70
Pouch distension (%)
60
50
40
30
20
10
0
No encounter Within 15min
15-60min
60-180min
180min-same
day
Individual Differences in Anti-predator Behaviours (Prediction D)
Vigilance: there was no difference between sex and age groups on the time spent
scanning the environment (Independent Samples t test: t18=0.653, P=0.522, for sex; One-way
ANOVA: F3,20=0.591, P=0.628, for age groups). However, rank categories differed in the
time animals spent scanning the environment (One-way ANOVA: F2,17=9.620, P=0.002,
partial η2=0.53). Medium rank individuals spent significantly less time surveying the
environment. No differences between low and high-ranking animals were observed
(PB>0.05). This behavioural pattern was attuned to the animal's exposure to predator risk
positions. Rank differences were found between the various amounts of time spent in safe
positions (One-way ANOVA: F2,21=8.211, P=0.002, partial η2=0.44). Medium rank
individuals spent high amounts of time in safe positions and consequently have less need to
monitor the environment. High-ranking individuals spent less time in safe places compared to
mid rank (PB=0.002). However, no significant differences were found in the amount of time
spent in safety between high and low ranking individuals (PB=0.318). Low and high rank
individuals did not differ in the amount of time they spent in safe places and consequently did
16
not differ in the amount of vigilance they invested. No significant differences were found
between the rank categories in the amount of time spent in unsafe positions (One-way
ANOVA: F2,21=0.819, P=0.455). Therefore, these results suggest no high-ranking advantages
and no low-rank disadvantages in terms of safety from predators.
Cheek pouch use: in line with the above results, no significant sex differences were
found in cheek pouch distension or filling when the subset of data that examined predator risk
was used (Independent Samples t test: t22=0.848, P=0.406 and t22=1.066, P=0.298 for pouch
distension and filling respectively). Similarly, no significant differences in pouch distension
or filling were observed between age-classes (One-way ANOVA: F3,20=1.505, P=0.244;
F3,20=2.155, P=0.125, for distension and filling respectively). Finally, the rank groups did not
differ in their observed cheek pouch distension or filling (One-way ANOVA: F2,21=0.710,
P=0.503; F2,21=0.503, P=0.612 for pouch distension and filling respectively).
Predator Risk and Cheek Pouch Emptying (Prediction E)
Baboons emptied their cheek pouches significantly more while in unsafe places.
Significant differences were found in pouch emptying by predator risk positions (Paired t test:
t23=4.67, P<0.001, d=1.53). Since cheek pouches were filled more in unsafe positions (see
Fig. 4), it is likely that this behavioural pattern reflects animals filling, emptying and refilling
their pouches. However, more interestingly, time spent in unsafe positions varied significantly
with the probability of encountering a predator (Paired t test: t12=4.595, P=0.001, d=1.93).
Baboons spent more time in unsafe places when the probability of meeting a predator was
low. In other words, animals avoided exposing themselves when the probability of a predator
encounter is high.
When the probability of encountering a predator was low, significant differences in
pouch emptying were found with predator risk position (Paired t test: t23=6.68, P<0.001,
d=1.82). Pouch emptying occurred more frequently in unsafe positions. However, the subset
17
of data to test pouch emptying by predator risk when the probability of a predator encounter is
high was too small. A Mann-Whitney U test on this data revealed no significant differences
(U=1.5, N1=2, N2=6, P=0.11, d=0.83). Assuming parametric data, available power to detect a
difference in the behavioural pattern (at the 5% level) between the conditions was very low
(14%). With the data here being non-parametric the true power is likely to be even less.
Discussion
Cheek Pouch Use in Relation to Food Distribution (and Contest Competition)
Cheek pouche use in the Mikumi baboons was related to food distribution. In
particular, cheek pouch use was more important for baboons when encountering clumped
food resources (i.e. animals filled, distended and emptied their pockets in association with
patchily distributed resources). However, for the Mikumi baboons during this study clumped
food was associated with lower levels of contest competition than dispersed food. This result
therefore does not provide support for the ICH hypothesis but is consistent with the PHR.
These findings are consistent with the literature in relation to cheek pouch use being
associated with clumped resources. Lindburg (1971) observed macaques (Macaca mulatta)
employ their cheek pouches while feeding on small food items which occurred in a patchy
fashion. Murray (1975) also refers to the frequent use of cheek pouches under clumped
conditions across genera. A similar pattern of pouch use was reported for Cercopithecus
ascanius and Lophocebus albigena (Lambert 1998; 2005) and finally, in captive Papio
cynocephalus (Lambert and Whitham 2001).
18
Captive studies have found intensive pouch use under crowded conditions. This has led
some authors to suggest that cheek pouches mitigate intragroup contest competition (Murray
1973; Deutsch and Lee 1991; Lambert and Whitham 2001). However, this assertion overlooks
other important factors that arise from the captive nature of these studies. That is, that
competition is not generated uniquely by the food per se, but by the predictability of food
absence during a set period of time. In captivity, food is usually only available at particular
time/s of the day, and therefore a food item if missed will only be restored during the
following feeding session. On the contrary, food availability in the wild is non-predictive.
Animals encounter resources under a continuous search fashion.
Cheek Pouch Use and Individual Characteristics
Cheek pouch use was not associated with individual characteristics of sex, age or
rank. These results are in line with previous studies that have examined rank in relation to
cheek pouch use. This again is consistent with the PRH and not the ICH.
Lambert (1998; 2005) found no sex effect on cheek pouch use in two cercopithecine
species: Cercopithecus ascanius and Lophocebus albigena. Hayes et al. reported some sex
differences in cheek pouch use. However, it is very difficult to draw a clear behavioural
pattern from the results. Analyses were computed for the various age groups as well as time
of the day, without reporting interactions between these variables. In addition, no overall
cheek pouch use comparison was presented for sex. There is no further support for sex
differences in the study of wild populations. Sex differences in cheek pouch use have only
been observed under captive conditions (Lambert and Whitham 2001). In this context, adult
females pouched food more often and to a greater extent than males.
Age differences in cheek pouch use in Papio ursinus were only apparent in males
(Hayes et al. 1992). The frequency with which males used cheek pouches increased with age,
peaking at the juvenile stage. However, no significant age differences were found in females.
In Lambert’s (2005) study, L. albigena age groups did not differ in their pouching of foods.
Although subadult C. ascanius males used their cheek pouches less than adult males, this
19
seemed likely to be the result of a difference in diet rather than a behavioural pattern per se.
That is, differential use of pouches may be explained by other factors such as nutritional
requirements.
Hayes et al. (1992) found that lower ranking adults (Papio ursinus) took no
advantage of their cheek pouches to reduce feeding competition costs. While female’s
dominance rank was not associated with pouch use, male’s dominance rank was positively
associated. That is, the higher rather than the lower ranking males were making greater use of
their pouches. Also, cheek pouch use was not associated with rank in wild living
Cercopithecus ascanius and Lophocebus albigena (Lambert 1998). Furthermore, no
significant rank effects on cheek pouch use were observed in Lambert and Whitham (2001)
despite the fact that this was a captive study. Lower ranking animals made more use of their
cheek pouchesbut no statistical rank effect was reported. Overall then, the primate literature
does not support the idea that cheek pouches provide rank related advantages.
Studies looking at the association between dominance rank and feeding success have
shown contradictory results. While some research has found a relationship between rank and
feeding success/time (Dittus 1979; Wrangham and Waterman 1981; Whitten 1983; Janson
1985, 1992; van Noordwijk and van Schaik 1987; Altmann and Muruthi 1988; Johnson et al.
1990; Saito 1996; Koenig et al. 1998: Presbytis entellus), others have not (Altmann 1980;
Barton 1989; Post et al. 1980; Ron et al. 1996). This may be a consequence of the differing
interpretations of the concept of dominance, a subject that has provoked considerable debate
in the literature (see Drews 1993 for a review). Nevertheless, those studies that do not find
clear feeding advantages may indicate that animals make use of alternative strategies to deal
with feeding competition. In this study, the lack of association between rank and cheek pouch
use, even during periods of food shortage, therefore eliminates one of the potential alternative
strategies that low-ranking animals may select to overcome contest competition costs.
20
Overall then, the results of this study very clearly do not support the intragroup
competition hypothesis. There was no evidence indicating that cheek pouches were used to
minimise the effects of contest feeding competition on animals. These anatomical features
seemed to be used to maximise food intake in relation to distribution of resources. In
particular, animals made use of their cheek pouches when resource items were distributed in
patches, in which food items cannot be monopolised once access to the patch has been gained.
The evidence in support of the intragroup competition function in the literature is based on the
finding that cercopithecines pouching foods did so to a greater extent when the number of
neighbours was higher (Lambert 2005). No other compelling evidence has been put forward
to date.
Baboons’ anti-predator behaviour was not fixed but individuals invested differentially
in accordance with their subjective perception of risk. Baboons avoided spending time in
unsafe places, but when this was inevitable, they were more vigilant. In addition, when
animals fed in dangerous positions, they filled their cheek pouches more frequently and to a
greater extent than when feeding in safer sites. The use of cheek pouches allowed the rate of
food harvesting to exceed chewing and swallowing rates, particularly consequential in case of
a sudden need to escape from a predator or to retreat to a safer spot to avoid unnecessary risk.
These results support previous suggestions made in the literature (Lindburg 1971; Richard
1985; Caldecott 1986; Lambert 1998, 2005).
Overall, no individual differences were observed in vigilance behaviours. Since the
analyses were conducted on all animals it is unlikely that the behavioural pattern was a
21
function of male competition. Furthermore, animals scanned the environment more frequently
when on their own (Gutiérrez Diego 2003 unpublished findings), when the individual risk is
higher, suggesting that vigilance was not attributable to the detection of other troops.
Although the exact target of the vigilant animal cannot be established (Treves 2003), the lack
of individual differences in terms of sex and age suggests that outward vigilance was an
important anti-predator behaviour for all individuals (Cowlishaw 1998; Steenbeck et al.
1999).
In contrast with previous studies (van Schaik & van Noordwijk 1988; Ron et al.
1996), higher-ranking individuals did not spend more time in safer positions. Consequently,
these animals engaged in vigilance as much as the lower ranks. Only medium ranking
baboons that spent more time in safer conditions invested less time in vigilance. Therefore, no
high-ranking advantages and no low-ranking disadvantages in terms of safety from predators
were observed. In line with other studies, no sex differences were observed (Cowlishaw
1998).
As with vigilance, no overall individual differences were observed in cheek pouch
use. No differences in pouch distension and pouch filling were detected between males and
females, age classes and rank categories. Since predation affects all individuals, the failure to
find individual differences in cheek pouch use provides further support for the Predation Risk
Hypothesis.
Baboons emptied their pouches more in unsafe places that were selected when the
probability of encountering a predator was low. Similarly, Lambert (2005) found that animals
that pouched food often stayed at the same location. While in these sites, animals may fillrefill their "pockets", therefore maximising foraging efficiency and avoiding the loss of the
resource in case of the need for urgent flight. Furthermore, foraging efficiency was not only
increased by pocketing foods while in unsafe places but also by incrementing food intake via
pouches after being faced with a predator.
22
There is no clear result in terms of what baboons do when they are exposed to a high
risk of predation. Although animals did not empty their pouches more in situations of high
risk, that they empty these in positions of safety cannot be ascertained due to the small
statistical power involved. In examining movement patterns after pouch filling,
Lambert (2005) found that irrespective of sex and age, animals either stayed in the
same place of acquisition or retreated to safer positions. Thus suggesting that animals
minimised predator risk by avoiding vulnerable positions. Since baboons, red tails and
mangabeys adopt behavioural patterns that should make them harder to capture, these results
are consistent with the hypothesis that cheek pouches serve an anti-predator function.
Vigilance was used in order to detect potential predators, whereas pouching foods enabled
minimisation of exposure and loss of resource in risky areas. Time investments in antipredator strategies were far greater for cheek pouch use. This however, is likely to be a
consequence of cheek pouches serving other functions (i.e. to minimise time constraints,
Gutiérrez Diego 2003 unpublished findings). Results also indicate that cheek pouches allowed
animals to 'catch up' with lower intake rates during days in which predators were encountered.
Murray (1973) suggested that low levels of predation lead to spacing mechanisms to
avoid within-group competition and in this case low levels of cheek pouch use is expected. If
on the contrary, predation pressures are high, spacing becomes less relevant than avoiding
predation. In this case, pouch use is expected to be high due to within group competition.
From this view, predation becomes a determinant factor of intragroup competition, which
may be mitigated by the use of pouches. Results from this study do not support this view in
that pouch use is not a function of within group competition, as it is independent of the effect
of intra-group competition and the kind of food available in high predation risk areas
(Gutiérrez Diego 2003 unpublished findings).
Thisresearch suggest that the Mikumi baboons used their cheek pouches to help
mitigate the foraging costs of anti-predation behaviourPocketing activities were more
23
important than vigilance from the point of view of time and energy investment. In this sense,
these anatomical features allow animals to behave as ‘energy maximisers’ since they facilitate
foraging efficiency, as well as to behave as ‘time minimisers’ since they permit food transport
and reduce time exposure in potentially risky areas. The use of cheek pouches allowed
animals to minimise the loss of food resources, otherwise in jeopardy, when entering
especially dangerous positions. Optimisation of the individual' fitness is therefore achieved
through the investment in adaptive responses to an unsafe environment.
The radiation of cheek-pouched monkeys took place in Africa and Asia
approximately five million years ago (Fleagle & Reed 1999), involving a great diversity of
habitats. In an attempt to explain the potential evolution of this anatomical trait, Lambert
(2005) notes that the use of cheek pouches by current cercopithecines suggests feeding
competition as the primary selection for cheek pouch evolution. However, habitat diversity
inevitably led to inter-regional variation in the diets and feeding ecologies of primates. This
may indicate that habitat as a single factor seems unlikely to have been the only selective
force in the evolution of cheek pouches (but see Maruhashi 1993). Yet, in the course of
evolution, predation is a problem that has affected cercopithecines in a more uniform manner
and may provide a more plausible explanation. Alternatively, the use of cheek pouches in
living populations may simply reflect by-products of a more general feeding/foraging
efficiency function.
As Lambert (2005) states, cheek pouches are a taxonomic trait that have received
surprisingly little attention in the primate literature. Despite the frequent use casually
observed by researchers, there is only a handful of published studies that have focused on this
anatomical structure (Hayes et al., 1992; Murray 1973, 1975; Lambert and Whitham 2001;
Lambert 2005). There is now data that suggests that cheek pouches play a role in dealing with
predation.
24
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