Sunday, August 15, 2010

Cheek Pouches: Cercopithecines' Arsenal for Global Domination

Cheek pouches are bilateral sacs on the lower cheek wall where food moves between the oral cavity and pouches through a slit-like opening (Lambert & Whitham, 2001). Most of us are familiar with cheek pouches in rodents, such as chipmunks, squirrels and hamsters. The cheek pouch is also one of the most important and distinguishing physical characteristics of the cercopithecines.

The cheek pouches of a White-tailed Antelope Squirrel. Most of us are much more familiar with cheek pouches in rodents than in cercopithecines. Photo on Flickr by J.N. Stuart.

A subfamily of the Old World Monkeys, cercopithecines range from Asia to sub-Saharan Africa and as far north as Gibraltar. Baboons, mandrills and macaques are examples of cercopithecines. According to fossil records, cercopithecines and colobines split between 12.5 and 10 million years ago. This suggests that the cheek pouch probably evolved at least 10 million years ago (Lambert & Whitham, 2001). The cheek pouch is present in all members of the cercopithecines but not in the colobines. While the exact adaptive function of the cheek pouch is unknown, numerous behavioral studies have been done on different cercopithecines to understand what the cheek pouch is selected for.

A rhesus macaque storing its food inside its cheek pouches. Photo from Garlyn Zoo.

Reducing Intraspecific and Interspecies Competition: 
A study with red-tail monkeys (Cercopithecus ascanius) and grey-cheeked mangabeys (Lophocebus albigena) in the Kibale National Park, Uganda showed that they were significantly more likely to use their cheek pouches in the presence of their conspecific (the same species) (Lambert, 1998). A subsequent study by Lambert (2005) with red-tail monkeys and grey-cheeked mangabeys also shows that both species were more likely to use their cheek pouches in the presence of greater numbers of conspecific.

A study of blue monkeys (Cercopithecus mitis stuhlmanni) by Smith et al. (2008) in the Kakamega Forest, Kenya shows that individuals are more likely to use their cheek pouch when their nearest neighbor is higher ranking than them.

Lambert & Whitham (2001) observed a group of captive yellow baboons (Papio cynocephalus) at a zoo and found that cheek pouches are mostly used when there are intense competition with their conspecific during main feeding time. Higher ranking individuals are less likely to use their cheek pouches compared to lower ranking individuals. The authors posit that the cheek pouches is an anatomical solution to maximizing energetic input while mitigating competitive intraspecies and interspecies competition.

Red-tail monkeys, like the one above, are more likely to use their cheek pouches in the presence of their conspecific and more so when the number increases.

Predator Risk and Avoidance: 
Lambert's (2005) study also shows that both red-tail monkeys and grey-cheeked mangabeys retreated to the safety of dense vegetation to process foods that were stored inside their cheek pouches. Lambert posits that this is a predator avoidance strategy.

A study of polyspecific association between Campbell’s monkey (Cercopithecus campbelli), spot-nosed monkey (Cercopithecus petaurista), and Diana monkey (Cercopithecus diana) from Taï Forest, Côte d’Ivoire shows that cheek pouches might be used to mitigate interspecific competition (Buzzard, 2006). Diana monkeys are the most frugivorous (ate fruits) while spot-nosed monkeys are the least frugivorous. Campbell's monkeys are more frugivorous than spot-nosed monkeys but less frugivorous than Diana monkeys. By comparing the cheek pouch distension of all 3 species, Buzzard found that Campbell's monkeys have the most cheek pouch distension overall, but had more distended cheek pouch when not near the highly vigilant Diana monkeys. Buzzard posits that the cheek pouch of Campbell's monkeys were the most distended as a response to predator risk and avoidance. Without the warning calls of the highly vigilant Diana monkeys, Campbell's monkeys stuffed their cheek pouch with food and retreated to a safer environment before they process their food.

Smith et al. (2008) posits that blue monkeys were less vulnerable when emptying their cheek pouch than filling them, therefore supporting the hypothesis that cheek pouch is selected for predator avoidance and reducing exposure to aerial predation. These blue monkeys (and most arboreal primates) retrieve to an area with high-density foliage and closer to the trunk of the tree to reduce exposure to predators.

Blue monkeys are less vulnerable when processing food in high-density foliage.

Storing Food, Resource Distribution:
Lambert's (1998) study also showed that red-tail monkeys and grey-cheeked mangabeys were significantly more likely to use their cheek pouches when feeding in clumped and high-quality resources (such as fruits).

Lambert & Whitham (2001) posit that the cheek pouches is an anatomical solution to maximizing energetic input while mitigating competition over limited food resources.

Smith et al. (2008) posit that cheek pouches use could also reflect the differences in the distribution of food resources (such as leaf feeding sites). Cheek pouches can be used to maximize foraging on extremely competitive resources.

An olive baboon feeding on the fruit of a Sausage Tree (Kigelia) in Manyara, Tanzania. Notice that she is stuffing her cheek pouches with the fruit. Photo on Flickr by Kibuyu.

Overall, cheek pouches in cercopithecines are used for more than one function and most probably varied between different species. Whether it is for interspecies/intraspecies competition, predator risk and avoidance or resource distribution, cheek pouches provide an added advantage for survival and are probably the reason why they were selected.

Buzzard, P. 2006. Rank and age related feeding strategy observed through field experiments in the Koshima group of Japanese macaques. Primates 47(4): 336-341. DOI: 10.1007/s10329-006-0188-6.

Lambert, J.E. 1998. A field investigation into the adaptive function of the cercopithecine cheek pouch. American Journal of Physical Anthropology 25(suppl): 145–146.

Lambert, J.E. 2005. Competition, predation, and the evolutionary significance of the cercopithecine cheek pouch: The case of Cercopithecus and LophocebusAmerican Journal of Physical Anthropology 126(2): 183-192. DOI: 10.1002/ajpa.10440.

Lambert, J.E. Whitham, J.C. 2001. Cheek Pouch Use in Papio cynocephalus. Folia Primatologica 72(2): 89-91. DOI: 10.1159/000049928.

Smith, L.W. Link, A. Cords, M. 2008. Cheek Pouch Use, Predation Risk, and Feeding Competition in Blue Monkeys (Cercopithecus mitis stuhlmanni). American Journal of Physical Anthropology 137(3): 334-341. DOI: 10.1002/ajpa.20879.


michellespidermonkey said...

Yay cheek-pouching! I worked on a cheek-pouching project when I was on Cayo--hopefully we will get the ball rolling on working on that manuscript. The abstract is in the AJPA supplement, from 2007 (I´d look for it and send it to you, but I´m at an internet cafe and don´t have my laptop...).

Raymond Ho, FCD said...

Yay! Please do Michelle. I find it quite hard to find cheek pouch studies of Asian cercopithecine species.