The Semantics of Vervet Monkey Alarm Calls: Part I

Anti-predatory alarm calls are important  for social animals to alert others of approaching predators. Without the presence of "language", some non-human primates are known to give out different predator-specific alarm calls to alert conspecific. These non-human primates include ring-tailed lemurs (Zuberbühler et al., 1999), white-faced capuchin monkeys (Fichtel et al., 2005), Diana monkeys (Zuberbühler, 1999), Campbell's monkeys (Ouattara et al., 2009) and vervet monkeys (Seyfarth et al., 1980).

Alarm calls are typically high frequency sounds because these calls are hard to localized by predators. On the other hand, low frequency sounds are easier to localized by predators. Calls that are hard to localized by predators are selected for because conspecific can pick up on the warning but predators cannot identify the location of the caller. If an individual successfully alert its social group of approaching predator yet does not reveal its location, it will significantly decrease the chance of the caller to be detected and increase the chance of its social group to avoid predation.

Vervet monkeys. Photo from Wikipedia.

Here, I will focus on the study of predatory alarm calls in vervet monkey (Chlorocebus pygerythrus) by Seyfarth et al. (1980) in the Amboseli National Park, Kenya. Vervet monkeys are Old World monkeys that range between Eastern and Southern Africa. These monkeys are diurnal and live in closely-knit social groups. They are quadrupedal and are both terrestrial and arboreal. Like all Old World monkeys, vervet monkeys have the characteristic cheek pouches that enables them to forage and store food to be eaten later. Male vervet monkeys have blue scrotal area and a red penis. Males and females are sexually dimorphic, with males slightly larger than females.

Male vervet monkey with blue scrotal area and red penis. Photo from Something Up Her Sleeve.

Vervet monkeys are known to elicit predator-specific alarm calls. Three well-documented vervet monkey alarm calls are those for leopard, martial eagle and python. Leopard alarm calls are short tonal calls produced in a series of inhalations and exhalations. Eagle alarm calls are low pitched grunt while python alarm calls are high pitched "chutters". Different alarm calls seem to evoke different responses to individuals that heard the alarm calls. However, the first reaction of a vervet monkey upon hearing an alarm call is to look at the direction of the caller. Looking at the direction of the caller gives them clues as to why the alarm calls were made and also where the caller is facing reveals the direction of the approaching predator. You can listen to these different alarm calls on this site.

As we said before, different alarm calls evoke different responses. Leopard alarm calls would make the monkeys run up into the tree to avoid being ambushed by the leopard. Also, these monkeys would sit on the branches further away from the tree because, even though leopards can climb trees, the branches could not support the leopard's weight. When an eagle alarm call is given, vervet monkeys would make them look up, run for the nearest bush or both to avoid an approaching aerial attack. Python alarm calls would the monkeys stand bipedally and look down on the ground.

A martial eagle. Photo by Jacques S G from Flickr.

Adult vervet monkeys are more discriminatory when eliciting alarm calls. Infants and juveniles calls however, are less discriminating as they attribute most terrestrial mammals with leopard calls, flying birds with eagle calls and stick-like figures with snake calls (although, compared to infants, juveniles are more discriminant when making alarm calls). In spite of that, adult vervet monkeys seem to elicit eagle alarm calls to different species of raptors and non-raptors (see illustration below). We can infer that adult vervet monkeys attribute eagle alarm calls to birds with the same silhouette as martial eagles. As vervet monkeys get older, they seem to have a better association between predator species and types of alarm calls. Vervet monkeys generally pay more attention to adult alarm calls than those of juveniles or infants.

Alarm calls made by infant, juvenile and adult vervet monkeys in response to sightings of birds of prey (raptors) and non-raptors. The number of calls cited for each age group refers to the total number of calls that were analysed (Gould & Gould, 1999). Click on illustration for larger view of the image.

The study of vervet monkey alarm calls by Seyfarth et al. (1980) laid an important ground work to better understand the complexity of animal communications. By showing that vervet monkeys make different alarm calls to different predatory species, we can posit that vervet monkeys have the ability to categorize different species. The ability to discriminate between terrestrial mammal, flying birds and snake-like objects starts during infancy in vervet monkeys. As they get older, they are better at associating predators with specific alarm calls.

An infant vervet monkey with its mother. Photo by Lip Kee from Flickr.

The ability to over generalize during infancy is evident in both vervet monkeys and humans. For example, upon learning the word "dog", human infants would refer to quadruped mammals they see as "dog". As the infant grows, so does the ability to associate the semantic meaning of words they learned. However, the acquisition of alarm calls in vervet monkeys is different than the acquisition of speech (language) in humans. Alarm calls in vervet monkeys are instinctual and not learned. Humans, however, have to learn their language. Failing to do so during the "critical period" generally will result in the inability to learn language in later years. Feral child are examples of human infants that lack linguistic input during their critical period of language acquisition.

Most of us interpret animal alarm calls as an uncontrollable auditory response to fear or pain, akin to humans yelping if we had our finger caught in a door. While this is not entirely false, some animal calls actually convey information from the caller to the listener. Seyfarth et al. (1980) posit that vervet monkey alarm calls are actually basic semantic signals or symbolic signals because each alarm calls seem to mean something to these vervet monkeys. While we don't know if these alarm calls actually mean "leopard" or "run up to the tree", we do know that it conveys specific information to their conspecific about approaching predators.

I will be blogging Part II of this post later this week, where I will explain in details the experiments done by Seyfarth and Cheney on vervet monkey alarm calls.

References:
Cawthon Lang KA. 2006 January 3. Primate Factsheets: Vervet (Chlorocebus) Taxonomy, Morphology, & Ecology. http://pin.primate.wisc.edu/factsheets/entry/vervet. Accessed 2011 March 9.

Fichtel, C. Perry, S. Gros-Louis, J. 2005. Alarm calls of white-faced capuchin monkeys: an acoustic analysis. Animal Behaviour 70(1): 165-176. doi: 10.1016/j.anbehav.2004.09.020.

Gould, JL. Gould, CG. 1999. The Animal Mind. Scientific American Library.

Ouattara, K. Lemasson, A. Zuberbühler, K. 2009. Campbell's Monkeys Use Affixation to Alter Call Meaning. PLoS ONE 4(11). doi:10.1371/journal.pone.0007808.

Seyfarth, RM. Cheney, DL. Marler, P. 1980. Monkey responses to Three Different Alarm Calls: Evidence of Predator Classification and Semantic Communication. Science 210(4471): 801-803.

Zuberbühler, K. Jenny, D. Bshary, R. 1999. The Predator Deterrence Function of Primate Alarm Calls. Ethology 105: 477–490. doi: 10.1046/j.1439-0310.1999.00396.x.

Zuberbuhler, K. 2000. Referential labelling in Diana monkeys. Animal Behaviour 59(5): 917-927. doi: 10.1006/anbe.1999.1317.

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.

References:
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 Lophocebus. American 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.