by Kevin Walker
Chabot College
1989
Introduction
This is a study of dominance behavior in three species of African Old World monkeys in captivity: Diana and hamlyn guenons, and the patas monkey. The three species presented an interesting contrast. The two guenon species are closely related, yet in the hamlyni group studied, the dominant individual was a female. The social structures of all three groups varied greatly, as did the habitats in which they lived. These factors provided for a wide range of behaviors, and although quite different, the groups did have some similarities.
Observations took place at the San Francisco Zoo between October 8 and November 19, 1989. On most days, the weather was unseasonably warm, and behavior was easy to observe. However, a major earthquake on October 17 disrupted activity at the zoo briefly, to the point that some animals escaped their habitats. Although behavior observed in the monkeys was greatly varied, the variation cannot be firmly attributed to the quake, since any number of other factors may be involved, and this researcher is not sufficiently learned in primate behavior to make such inferences.
METHODOLOGY
The dominant monkey in each group was studied for six individual behaviors: Feeding, play (social and solitary), displays, (verbal and visual), grooming (social and solitary), rest, and sexual activity. Each monkey was observed for two periods of 3 hours and 40 minutes each. At 10-minute intervals, the prevalence of each behavior was recorded, and the total number of occurences was later tallied. By comparing the number of times the individuals performed each behavior, it was possible to compare their dominance roles. The way the individuals performed each behavior was also analyzed, and differences between species were also considered.
This research was limited by at least two factors. First, it cannot be effectively applied to monkeys in the wild since those in captivity tend to be more docile, as well as severely restricted in their movement. Although the sizes of the habitats were quite large, they cannot compare to the open range. Patas monkeys, especially, normally have a much larger home range. Some field studies are discussed. Secondly, it was impossible to observe all behavior. There were many places out of view in the habitats; and at night, the monkeys were taken to indoor sleeping quarters.
Background: Cercopithecines
TAXONOMY
HISTORY
The only Ogliocene remnants come from the Fayum site in Egypt. Findings there have suggested a possible primitive subfamily of Cercopithecidae called Parapithecinae. The ecology at the time was probably lowland tropical rainforest. Some Miocene finds suggest possible monkey ancestors, perhaps Dryopiths. The first finds of definite ancestors of Old World monkeys come from Pliocene Asia. It has been suggested that Cercopithicines either evolved in Asia and migrated to Africa, or evolved simulateously on both continents.1
CHARACTERISTICS
Old World monkeys, (subfamily Cercopithecinae), are distributed throughout Africa and southern Asia. For this study, only African Cercopithecines were chosen. The African Cercopithecines are the most widely distributed of all primates. Guenons alone have more species and forms than any other primate genus. Cercopithecines are the most common, most diversified of the primates.
Several characteristics are shared by the Cercopithecines. All are quadrupedal and most are arboreal, (except the patas monkey, along with baboons and macaques). Cercopithecines are more generalized than most primates. They are largely omnivorous and diurnal, and some type of stable social organization can be found in every species. All utilize a sitting posture, which has produced hard underside pads called ischial callosities. Often called "thin-nosed monkeys," their thin nose bridges and lack of frontal sinuses differentiate them from New World, or "broad-nosed" monkeys. They have a powerful, jutting facial bone structure, with cheek pouches and a longer auditory canal. Flat nails are on all fingers and toes. At birth, they are more mature than any other hominoid.
Exceptions to their homogeneity are tail length, secondary sex differences and coloration. All three traits fluctuate greatly from species to species. Sexual dimorphism is especially pronounced in the terrestrial species, including patas monkeys.
Background: Guenons
The two species of guenons, (genus Cercopithecus), observed were hamlyni and diana. Hamlyni guenons were first described by Pocock in 1907, and dianas by Linnaeus in 1758.
Both species are distributed in west Africa, the hamlyni being concentrated mainly in the eastern Congo basin. They are both arboreal, and live primarily in the middle to high strata of the rainforest, seldom descending. Their enemies include wildcats, pythons and large birds of prey. Several special adaptations allow them easy evasion and camoflage, as discussed in the observations.
In the wild, both species are mostly frugivorous. Dianas also eat seeds, nuts, young shoots and buds. Hamlyns have been observed eating insects and even other small animals, such as lizards. Wild guenons dwell in large groups, contrary to their cousins in captivity. Hamlyn groups number around 10, but diana groups have been known to approach 50. Both groups have only one or two adult males and a few adult females; the young make up the largest portion. Life expectancy is up to 26 years. Females bear young at 4.5 to 5 years, and gestation lasts 6.5 to 7 months. Background: Patas Monkey Erythrocebus patas, the patas monkey, is also called the Military monkey, Sergeant-Major monkey and Hussar monkey. There are four subspecies: Patas, villiersi, pyrrhonotus and baumstarcki.
The patas is sometimes refered to as a guenon, and even grouped under the genus Cercopithecus. There are several adaptations that effectively separate the patas from guenons.
Most importantly, the patas is adapted for terrestrial locomotion. It roams the savannah areas north of the equator in Africa. The patas' limbs, hands and feet are more specially adapted for running on the ground, and this puts it closer, taxonomically, to baboons than guenons. It seems to fall somewhere between guenons and baboons.
Patas monkeys in the wild are very mobile. Their home range is up to 30 square miles, and they travel up to seven every day. This is due to the arid environment and wide dispersal of food. They eat consistently throughout the day, (grasses, fruits, insects, seeds, mushrooms, sometimes small lizards), often while walking. They are the fastest primates, capable of speeds of up to 35 miles per hour. Their agility, combined with silence, alertness and ingenious evasion tactics, allow them to escape such predators as jackals, hyenas, leopards and eagles.
Their long limbs and small hands and feet allow them to pick up tiny insects and seeds in grasses 3 to 13 inches high. They live in one-male groups of 5 to 25, averaging about 18. A study at Murchison Falls National Park found groups up to 31, as well as a few solitary males, and one group of four males.2 Females give birth at about five years, and infants are usually born in the first six months of a year. Unlike other Cercopithecines, there is no swelling or color change during the 30-day cycle, and the only overt sign is menstruation.
Observations: Hamlyns
The hamlyni group at the San Francisco Zoo consists of two females and three males. The only adult is a female, and she presides over the group. Her exact age is not known, but Primate Keeper Carol Martinez estimates her to be "at least six." The other female is approximately 2 years old, and the males are about 2, 3 and 4. All were found in the wild, which is why ages are estimated.
All the group members are roughly the same size, about the size of a house cat. (Hamlyns range from 43 to 47 inches long; their tail is about half that length. They weigh 13 to 18 pounds). Their short, thick fur has a "back-to-front" coloration pattern. The head, neck and body are a speckled olive grey, and the underside, legs and arms are black. The tail is silvery-grey. Their most distinctive marking is a pair of white stripes, across the brow and down the ridge of the hooked nose. Not only does this allow them to recognize eachother in a dim forest, it also makes them look like an owl, as does the shape of their face. They have, hence, been given the common name "Owl-faced monkey." This species was once thought nocturnal, but this has proven incorrect.3
In this group, the adult female, and one of the smallest young, are a bit more brownish than the others, which would seem to indicate they are immediate family. This, however, is not known. It could be that the adult female devotes more time to it because of their color similarity.
Their zoo habitat is a rather small, enclosed cage that has, as its base, a slope made of rock and dirt. A long, dead branch sits diagonally on the slope, and at the top, a dry plant sprouts from the rock. Smaller twigs and sticks litter the dirt, and in the center of the cage, a rope net is stretched across. Alas, it is not a very convincing upper rainforest recreation.
The net seems to be the monkeys' favorite piece of furniture, and they seem to enjoy climbing the cage walls and doing acrobatic backward dives into it. It also provides something to chew on when there's no food. They are fed in the afternoons, fruit and leaves. They also chew on the plants within the cage. Food is chomped with large canines, and sometimes stored in buldging cheeks.
The adult female clearly presides over the young, but not overtly. She is older and more experienced, and they seem to respect her. The young sometimes taunt her, and occasionally try to steal food from her, but she does scold them when she feels they've gone too far. It can be described as a "low-grade" domination. She acts as a mother most of the time.
The three males are still quite young, and they play vigorously. Only once did a male try to mount the adult female; he didn't suceed. The males are simply too young, and have no older male to observe...or do they? These monkeys have full view into neighboring cages. Although at no time were they observed associating with any neighboring "prisoners," they are free to spy on the activities of the Lion-tailed macaques on one side, and a large, lively group of Francois' Leaf monkeys on the other.
The adult female's dominance role was most easily observable during times of feeding and social grooming. In a few instances, she would threaten young ones trying to steal her food. Only once did she actually give chase. When she, or any of the others, got angry, the fur around the face would stand on end, and the head would bob, enhancing the owl look. This was often accompanied by a raspy chatter or all-out scream.
Grooming was mostly solitary. The adult female did groom the brownish young one, but they did not spend so much time together as to merit a parent-child relationship. She was seen grooming this young one once, after it initiated; she also groomed the young male that had tried mounting her.
The overall setting was not very family-like. Although she was respected as the dominant figure, the others were almost her size, and seemed more interested in playing with eachother. She made no few attempts to join in the fun, opting instead to munch on a twig, or simply sit near the top of the cage, feet in front, unmoving. It should be noted, however, that when she did move around, she was certainly no sloth. Her acrobatic leaps and whirls were by far the most impressive; and the younger ones often took notice. In all the monkeys, the hands were very adapted to arboreal movement, and the tail used for balance and aerodynamics.
Observations: Diana
The smaller group of diana guenons has a cage about three times the size of the hamlyns'. Much more resembling a tropical rainforest, this setting includes several large plants, various logs and branches, and denser foliage that, unlike the hamlyni habitat, has places to hide, (from people and other dianas). It is similarly set on a slope inside an enclosed cage, but contains much more room and foliage, as well as two nets and some ropes stretched across the upper portion. It is possible that the hamlyns ate most of their foliation, but it's highly unlikely they ate up more room or more "furniture".
Three dianas live here, one 18-year-old male and two females, 14 and 8. This would seem advantageous to the male, but he showed little enthusiasm. This could be attributed to his age, or any of several other factors.
A bit larger and chubbier than the hamlyns, these guenons also have longer tails, longer than their bodies. Their ischial callosities, like the hamlyns, are quite small, and their fur is similar in length and thickness but not color. The dianas are brighter, perhaps to aid in recognition in a darker, denser forest; or perhaps because there are fewer predators in their native habitat; perhaps both. The chin-chest area and the front of the arms are a creamy white color. The back is medium to dark brown, and the hind and inner flanks, chestnut brown to yellow. On the outside of the hind legs are the distinctive, white, arched lines that give them their name, after Diana, "Goddess of the Hunt." The face also sports a short white beard. All three in this group are similar in coloration and size; the male, however, is distinguishable by a slight tinge of grey down his back.
All three move gracefully, with supple, feline-like movements. They climb, run and jump easily, using their tails for balance. They eat frequently, green leaves and shoots. They are fed fruit and leaves in the afternoon, (like all other monkeys at the zoo).
The male is dominant, but in a low-grade way similar to the hamlyn adult female. He doesn't associate much with the females, but when he does, he firmly asserts his role. All the aggression displays he put on, (all food-related), were loud and threatening. Once, he actually threw his meal at a female that tried to make off with some scraps, yelling at her with chatters and cries. His tail was raised and head lowered.
Aside from the few aggressive episodes, he was quite friendly toward the females, and was not without sexual activity. The females "presented" to him a few times, and he declined only once. Sex always took place on branches or bars. Play was much more common than sexual activity. The three seemed to enjoy eachother's company as they chased eachother and performed for the human spectators. Solitary play was more common, and usually involved a twig or rock being batted around.
The most interesting behavior observed was food-related. The male would go to the bottom edge of the cage and reach outside for leaves of the surrounding bushes. He would do this even when food was plentiful in the cage. The outside leaves seemed a delicacy, and whenever he would succeed in obtaining a few, the females would anxiously plead him for some by grooming him, then casually reaching for the food. He realized the value of the leaves, and firmly scolded them. After all, it seems he was the only one who could reach them. He was not completely without feeling, and would always drop a few leaves for the females, then go to the top of the cage to eat in peace. It all seemed very symbolic -- the leaves as objects of power.
The male often dropped other kinds of food, and it seemed more messiness than sympathy. He was a wasteful eater, often taking a few bites and discarding the rest. DeVore (1965) noted similar behavior in guenons in the wild.4 Feeding always took place on branches or bars.
Grooming was mostly solitary, and there was little initiation. When initiated, however, it was very thorough. The females were involved in grooming far more than the male, but seemed to groom him more thoroughly. In fact, the females spent a lot of time together, while the male ate or groomed himself. But overall relations between the three were generally good. His dominance role was clear, and he seemed content to rest on a branch, legs stretched out in front of him.
Observations: Patas
The patas troop has, by far, the largest and most diverse habitat of the three groups studied. Although small compared to natural patas territory, the San Francisco habitat seems a good re-creation of the African savannah. The large landscape is surrounded by a high cement wall, and is open on top. It contains several barren trees, all kinds of bushes, grass and other foliage, rocks, hills, and so on.
There is one adult male, 13 years old. He is accompanied by four females, three of them 11, one 13. The patas monkeys, adapted for terrestrial life, have strikingly different features than the guenons observed.
They are the size of a small to medium dog, with similar proportions. They range from 23 to 34 inches in length, with a 50- to 75-inch tail, and weigh up to 53 pounds. Sexual dimorphism is quite distinct: males are more than twice the size of females. This is apparent early on: An 18-month-old male is the same size as a 42-month-old female. The males also are distinguishable by their fierce-looking canines, their bright blue scrotum, and longer fur around the shoulders and neck. Males and females alike are slender, with long arms and legs. Hands and feet are adapted for terrestrial movement and thus much smaller than those of guenons. Color varies between individuals and sex-age classes. Generally, the crown of the head, nape, back and sides are red to brown or light brown, (mixed with grey in older males). The underside is much lighter: Pure white in males, light brown in females and young males. The face is dark grey to black, with a white "mustache," which led to their common name "Military monkey". Infants are a darker brown, and change color at about three months.5 In the observed group, the females seemed quite light compared to the male, who was darker and more reddish. The patas' color camoflages them well.
Not surprisingly, most movement took place on the ground, in the form of walking, cantering and galloping. In play-chases, the patas demonstrated their agility with quick changes of direction, bounces off trees, and easy scurries around bushes. Climbing up trees was fairly frequent but rather slow; the patas' look ground-adapted even when in trees.
The social structure was the most pronounced example of male dominance observed. The dominant male is accompanied by an "alpha" female; that is, she is "second-in-command". She receives most of his attention, and was clearly chosen by him. A further hierarchy was not observable among the other females, but the one described was quite prominent.
The male guarded his kingdom very attentively. He often took on a "watchdog" role, stalking around the perimeter or scanning the area from a treetop. In the wild, in the event of danger, the male will put on an elaborate diversionary display in which he flashes his white thighs, then vocally scurries off in one direction while the rest of the pack goes in another.6 No such behavior was observed in this study.
In correlation with Hall's field study, (1968), the patas troop seemed to be most active in the morning.7 Play-chases and sexual activity occurred steadily until noon or 1 p.m., when the temperature rose. Then came an hour or two of rest, when mostly grooming took place. Ironically, it was during times of rest that the dominance hierarchy was most visible.
Female social status seemed to be measured by sitting distance from the male. The "alpha" female was invariably always closest to the male. Most grooming of the male was done by the "alpha" female. Others were allowed to do it, but with much less frequency. The male himself did little grooming, and his grooming was short and cursory. When reciprocal grooming occurred between the male and "alpha" female, the other females took great interest. When it was finished, they would meagerly appraoch the both the male and female, and attempt to groom. Sometimes they were reciprocated, sometimes not; (the "alpha" female reciprocated more often). Grooming seemed to be the most frequent behavior throughout the day, occuring more in the morning than afternoon.
Feeding patterns seemed steady throughout the day, yet during the hotter hours after noon, it seemed to slow. The male, of course, always had the most and best food, and shared it with the "alpha" female only. He only allowed her to have small pieces, however. When she attempted to grab a large piece of fruit or piece of vegetation, he would threaten. Feeding always occurred on the ground, in sitting positions or while walking. Once, the male grabbed for a flying insect, balanced on his hind legs. Drinking of water was quite infrequent.
Most social play took place between the females. It was mostly in the form of chases, and some wrestling. The tempo seemed to build until both individuals collapsed to rest under a tree or bush. When the male was involved in play, it almost always involved sex. Other females seemed to know this, and sat up and took notice whenever the male initiated a chase. Once, he chased all four females at once. They scattered, and taunted him individually, and he soon became frustrated, and took to a treetop. When he did catch a female, or when a female "presented" to him, he readily mounted. Incidentally, Keeper Carol Martinez informed that the male was, in fact, neutered.
Strangely, most aggressive behavior was by the females. They sometimes snarled at eachother for no apparent reason. The main reason, undoubtedly, was over the male, and the "alpha" female frequently tried to chase away any female that approached the male. But otherwise, the females were quite friendly, and when they approached eachother, they often touched lips, as if kissing. The females also initiated group movements, and not necessarily the "alpha" female. If two or more females settled in one place, the male would follow, then the rest.
When the male became aggressive, he was usually stalking a female to mount, when another would try to gain his attention. He always remained quiet, as did the others. This is part of their adaptation in the savannah. Throughout the entire observation period, only one or two vocalizations were heard.
Comparisons
The three species provided three very different types of dominance behavior. There emerged distinct personalities of individuals, if not species. The hamlyn group provided an example of a sort of "mother with teenagers"; The diana provided a kind of "happy, subdued husband with two wives"; and the patas was an example of a "true king, a military-thinking, self-centered, absolute ruler" .
Various factors may be at work to form such disparate rulers. One may be the species size proportions. The guenons were very close in size, whereas the dimorphism in the patas' may simply trigger a dominance perception -- indeed, the "biggest kid on the block".
Habitat size could also play a part. From hamlyn to diana to patas, habitats get progressively larger. Granted, the patas utilizes a much larger home range, and of course all three species would no doubt act completely different in a natural setting; but could it be that, to rule a larger land takes a firmer hand? Indeed, social hierarchies did seem to grow with each habitat; a secondary ruler was present in the patas group.
Food supplies also increased with each group. The hamlyn "mother" was much more apt to give scarce food to her young, whereas the patas "king" would scarcely sacrifice a morsel, except to his "queen". ("Let them eat cake!") The diana "husband" was very wasteful with his food, probably knowing he would get more. Then there were the "power" leaves he used to control his "wives". The whole picture is easily likened to human social class struggles.
By comparing data collected, the following trends emerge: The patas ruler had by far the most displays, and spent the most time at play and in grooming. The diana ruler spent the most time at rest, but had an equal number of sexual encounters as the patas; the hamlyn ruler had no sex at all. The patas spent most of its time grooming, while the others spent most feeding. All three, coincidentally, spent equal time feeding.
There were other similarities, in the way the three rulers ruled. The number-one rule for all three seemed to be "serve yourself first". The dominant individual always got first and best selection of food and places to sit or eat. All three also seemed to know when to use aggression, usually when it was a last resort. They all used food to manipulate and control their underlings. And the dominant figure was always groomed well.
Considering, the disparities of the three groups, the similarities are quite clear. They illustrate how power is used in different situations, and in conclusion, they seem to correlate well with human behavioral patterns.
1. Simons, Elwyn L. (1970). "The Development and History of Old World Monkeys." In Napier, J.R. and Napier, P.H. (Eds.), Old World Monkeys: Evolution, Systematics and Behavior (p. 97). London: Academic Press.
2. Hall, K.R.L. (1968). "Behavior and Ecology of the Wild Patas Monkey, Erythrocebus Patas, In Uganda." In Jay, Phyllis C. (Ed.), Primates: Studies in Adaptation and Variability (p. 32). New York: Holt, Reinhart and Winston.
3. Napier, J.R. and Napier, P.H. (1967). A Handbook of Living Primates (p. 100). London: Academic Press.
4. DeVore, Irven. (1965). Primate Behavior: Field Studies of Monkeys and Apes (p. 104). New York: Holt, Reinhart and Winston.
5. Hall, K.R.L. (1968). "Behavior and Ecology of the Wild Patas Monkey, Erythrocebus Patas, In Uganda." In Jay, Phyllis C. (Ed.), Primates: Studies in Adaptation and Variability (p. 38). New York: Holt, Reinhart and Winston.
6. Ibid., p. 74
7. Ibid., p. 32
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Thanks to Prof. Susan Landes, for whose introductory course this was assigned.