Competition predation and the evolutionary significance of the cercopithecine cheek pouch The case of Cercopithecus and Lophocebus.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 126:183–192 (2005) 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 KEY WORDS ecomorphology Kibale National Park; Uganda; frugivory; guenons; mangabeys; Miocene; ABSTRACT 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 © 2004 WILEY-LISS, INC. *Correspondence to: Joanna E. Lambert, Department of Anthropology, University of Oregon, Eugene, OR 97403. E-mail: firstname.lastname@example.org Received 8 January 2002; accepted 31 October 2003. DOI 10.1002/ajpa.10440 Published online 27 July 2004 in Wiley InterScience (www. interscience.wiley.com). 184 J.E. LAMBERT 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). CHEEK POUCH USE IN FOREST CERCOPITHECINES 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. METHODS 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, 185 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 186 J.E. LAMBERT 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 CHEEK POUCH USE IN FOREST CERCOPITHECINES 187 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. RESULTS 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 ⬍ 0.01). 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). 188 J.E. LAMBERT 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. DISCUSSION 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 CHEEK POUCH USE IN FOREST CERCOPITHECINES 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 competition? 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 189 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). 190 J.E. LAMBERT 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) High Large ratio ⫽ 0.37 Erythrocebus Low Medium ratio ⫽ 0.31 Cercocebus/Lophocebus High Large ratio ⫽ 0.37 Macaca High Big ratio ⫽ 0.4 Cercopithecus 3 2 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) Female relationships (8) Variable; but usually large Variable; but usually large Variable; but usually large Large Resident/egalitarian Resident/egalitarian Resident/egalitarian Resident/nepotistic Theropithecus Low Small ratio ⫽ 0.19 One resident male Small Resident/nepotistic Papio Variable Small ratio ⫽ 0.25 Variable, but typically ⬎1 resident male Large Resident/nepotistic Female competition (8) Low WG High BG Low WG High BG Low WG High BG High WG Low BG High WG Low BG High WG Low BG 1 There are too few data on cheek pouch frequency among Cercopithecinae to give absolute frequencies; this variable is thus presented on a relative scale. 2 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). 3 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 resources. 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- CHEEK POUCH USE IN FOREST CERCOPITHECINES 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. ACKNOWLEDGMENTS 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. 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