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Cheek Pouch Use, Predation Risk, and Feeding Competition in Blue Monkeys (Cercopithecus Mitis Stuhlmanni)

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Cheek Pouch Use, Predation Risk, and Feeding Competition in Blue Monkeys (Cercopithecus Mitis Stuhlmanni) AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 137:334–341 (2008) Cheek Pouch Use, Predation Risk, and Feeding Competition in Blue Monkeys (Cercopithecus mitis stuhlmanni) Lindsey W. Smith,1,2* Andres Link,2,3 and Marina Cords2,4 1Department of Anthropology, City University of New York Graduate Center, New York, NY 10016 2New York Consortium in Evolutionary Primatology (NYCEP), New York, NY 3Department of Anthropology, New York University, New York, NY 4Department of Ecology, Evolution and Environmental Biology, Columbia University, New York, NY KEY WORDS Cercopithecidae; foraging strategies; Kenya; predator avoidance; nearest-neighbor dominance score ABSTRACT The adaptive function of cheek pouches gated several measures of competitive threat, but only in the primate subfamily Cercopithecinae remains unre- one supported the competition-reduction hypothesis: solved. By analyzing the circumstances of cheek pouch when the nearest neighbor’s rank increased, subjects use, we tested two hypotheses for the evolution of cerco- were more likely to increase than to decrease cheek pithecine cheek pouches proposed in earlier studies: (1) pouch use. Overall, our findings supported the preda- cheek pouches reduce vulnerability to predation, and tion-avoidance hypothesis more strongly than the com- (2) cheek pouches increase feeding efficiency by reduc- petition-reduction hypothesis. We suggest that variation ing competition. We studied two groups of wild blue in cheek pouch use may reflect differing behavioral monkeys (Cercopithecus mitis stuhlmanni) in the Kaka- strategies used by cercopithecines to mitigate competi- mega Forest, Kenya, conducting focal observations of tion and predation, as well as factors such as resource feeding individuals. Monkeys were less exposed while size and distribution, home range size, and travel pat- emptying their cheek pouches than filling them, sup- terns. Am J Phys Anthropol 137:334–341, 2008. VC 2008 porting the predation-avoidance hypothesis. We investi- Wiley-Liss, Inc. Although cercopithecine monkeys are distinguished C. diana) in the Tai National Park, Coˆte d’Ivoire, Buz- from other primates by the presence of cheek pouches in zard (2006) reported that C. campbelli had less dis- which they temporarily store and begin to digest food tended cheek pouches when feeding in association with (Murray, 1975), the adaptive function of cheek pouches C. diana than when feeding without C. diana, a pattern has not been conclusively determined. As Lambert that supports the predator-avoidance function of cheek (2005) noted recently, few studies have quantified cheek pouch use if mixed-species associations reduce the risk pouch use and related it systematically to environmental of predation (Wolters and Zuberbu¨ hler, 2003). or social variables that might shed light on its adaptive Support for the competition-reduction hypothesis has function. Even fewer studies have been conducted on pri- been somewhat mixed. Hayes et al. (1992) found that all mates living in natural environments. We aimed to test age-sex classes of wild Papio ursinus in the Mkuzi Game two nonexclusive hypotheses about cheek pouch use sug- Reserve, South Africa, used their cheek pouches more gested by earlier research, using detailed observations of frequently during mid-day periods when they spent most the foraging behavior of wild blue monkeys (Cerco- time feeding and the potential for competition was high. pithecus mitis stuhlmanni). Cheek pouch use may (1) Additionally, cheek pouch use decreased with advancing reduce vulnerability to predation by allowing quick ac- age for both males and females, and adult females used quisition of food and retreat to safer positions to process their cheek pouches more than males did. Although food, and/or (2) increase feeding efficiency by reducing these results are consistent with the idea that competi- intra and/or interspecific feeding competition. These hypotheses derive from the facts that primates forage gregariously and often in polyspecific associations (which Grant sponsor: New York Consortium in Evolutionary Primatol- can foster competition both within and between species) ogy (NSF IGERT Grant); Grant number: 0333415; Grant sponsor: and that they are frequently vulnerable to predators NSF; Grant numbers: 9808273, 0554747; Grant sponsor: AAAS Grant. while foraging (Murray, 1975; Lambert, 2005). Supporting the predation-avoidance hypothesis, Lam- *Correspondence to: Lindsey Smith, Department of Anthropology, bert (2005) reported that Cercopithecus ascanius and CUNY Graduate Center, 365 Fifth Avenue, New York, NY 10016. Lophocebus albigena in the Kibale National Park, E-mail: [email protected] Uganda, retreated to safer places after filling their cheek pouches. Furthermore, L. albigena lived in smaller Received 16 December 2007; accepted 9 May 2008 groups (suggesting reduced within-group feeding compe- tition), yet they used their cheek pouches more fre- DOI 10.1002/ajpa.20879 quently than C. ascanius (Lambert, 2005). In a study of Published online 8 July 2008 in Wiley InterScience three wild guenon species (C. campbelli, C. petaurista, (www.interscience.wiley.com). VC 2008 WILEY-LISS, INC. CHEEK POUCH USE IN BLUE MONKEYS 335 tively disadvantaged individuals use cheek pouches most The forest’s native vegetation is a semideciduous type often, the effects of dominance rank in males appeared of Guineo-Congolian lowland rainforest (Cords, 1987), contradictory: higher-ranking males used cheek pouches and the study site includes primarily this type of vegeta- more frequently than lower-ranking males. Among adult tion in near-natural and secondary stages (Lung, females, however, there was no relationship between 2004). Blue monkeys at Isecheno are sympatric with C. rank and cheek pouch use (Hayes et al., 1992). ascanius, Colobus guereza, and Perodicticus potto (Cords, Lambert (2005) found that L. albigena and C. ascanius 1987). They occur at a density of 220 individuals/km2 (5 used cheek pouches more often when feeding on more groups/km2; Fashing and Cords, 2000), a relatively high contestable foods (namely fruits), and when in the pres- density for the species (Lawes et al., in press). The two ence of a larger number of conspecifics. There were no study groups had neighboring home ranges of approxi- age-sex class differences in cheek pouch use among L. mately 19 ha (GS) and 16 ha (GN), including a six hec- albigena, but C. ascanius subadults used their cheek tare area of overlap. pouches less than adults, perhaps because the subadult The two groups originated from a single parent group diet included more insects, a food less likely to be placed that had been studied intermittently since 1993 and con- in cheek pouches (Lambert, 2005). Studying captive tinuously since 1997. The parent group split into GN adult Papio cynocephalus, Lambert and Whitham (2001) and GS in 1999. In 2004, when we conducted our study, found that cheek pouch use increased when the animals GN included 10 adult females, five juvenile males, and were provisioned and competitive interactions were fre- two juvenile females, while GS had 19 adult females, six quent (also Hannibal and Rodrigues, 2007). In addition, juvenile males, and nine juvenile females. Each group lower-ranking animals used their cheek pouches more also included just one resident male, the modal number than higher-ranking animals, and females used cheek for the species (Cords, 2000a). Our subjects included all pouches more than males. These results support the group members over the age of 2 years. All subjects competition-reduction hypothesis, although they differ could be individually recognized based on physical from the study of P. ursinus with respect to dominance features. effects (Hayes et al., 1992). Lambert and Whitham (2001) found that, overall, cheek pouches have been used more often in captive Data collection baboons than in wild ones (59% vs. 28% of feeding We collected data from our study groups between 0700 records), and they suggested that the extremely clumped and 1800 h from June 27 through August 14, 2004 (31 food available in captivity leads to a reliance on cheek observation days for GS, 21 observation days for GN). pouches to minimize within-group contest competition We conducted focal animal samples, making instantane- for food. Hayes et al. (1992) noted similarly that cheek ous records at 2-min intervals. Focal subjects were never pouch use in wild baboons varied with the distribution of sampled more than once per day to maximize independ- food. Their study, conducted at a time of year when food ence of samples. We also tried to maximize the time was clustered in fruiting trees, revealed a higher fre- between samples of each subject by rotating through quency of cheek pouch use than previous observations of most group members before resampling any one of them. wild baboons eating more widely dispersed foods such as Focal samples began when the subject started to ingest grasses and roots (Altmann and Altmann, 1970). More food and lasted 20 min if no cheek pouches were filled, clumped food is often viewed as enhancing the potential or past the 20-min mark if cheek pouches were filled for competition. (see later). Sometimes feeding activity was continuous We investigated the influence of predation risk and during the entire sample, whereas in other cases it was intraspecific competition on cheek pouch use in two interrupted by other activities such as resting or groom- groups of wild blue monkeys (C. mitis stuhlmanni) living ing. With the exception of the description of the subjects’ in adjacent and partially overlapping home ranges. Blue diet during our study, our analyses included only those monkeys are primarily arboreal, forest-dwelling omni- samples in which feeding occupied at least half of the vores, although their diets consist mainly of fruits, leaves, initial 20 min. The average number of such samples per and to a lesser extent, invertebrates (Cords, 1987; Lawes, individual was 3.9 6 1.4 for 18 subjects in GN, and 5.1 1991; Chapman et al., 2002). We tested the predation- 6 2.2 for 35 subjects in GS. Total focal sampling dura- avoidance hypothesis by comparing the exposure of ani- tion was 73.5 h for GS and 25.5 h for GN.
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