Fighting Fit

Some red colobus monkeys in estrus are uninhibited,  unintimidated, and unconventional in their mate choices.

Mr. Mean, the number-two male, snuck off from the troop with his favourite sexual partner for uninterrupted sexual activity.

Photographs by Dawn Starin

One hot, rainy June morning in the Abuko Nature Reserve in the West African country of The Gambia, a troop of western red colobus monkeys, Procolobus
badius temminckii
, moved out of their early morning feeding trees. Dropping fruits, feces, urine, and broken branches along the way, sexually receptive females raced ahead through the trees toward the shade of the dense raphia palm swamp—followed closely by the dominant male, with subadults, juveniles, mothers and clinging infants bringing up the rear. The entire forest—nearly 107 hectares—reverberated with the sounds of females screaming as they threw themselves from branch to branch, announcing that the mating season had arrived. The trigger that initiates this collective, elevated level of sexual activity in red colobus monkeys is unknown. Most theories suggest that environmental conditions are responsible—the onset of the rains, a rise in humidity and temperature, a diet rich in specific fruits and flowers, and/or an increase in day length.

An adult female (left) grooms an adult male. Sexual dimorphism is virtually non-existent in the western red colobus. In fact, the largest adult in the focal troop was a female and one of the smallest adults was a male.

During the mating season, females, around three years in age and older, sport genital swellings for about five days each month. These conspicuous bulges presumably signal that the female is fertile and sexually receptive. And females do their utmost to advertise their readiness. First, they run around screaming to attract males within range, then they adopt postures that show off their swellings to the greatest advantage. These audiovisual displays are contagious—if one female displays, it sets off a chain reaction: all the sexually receptive females in the troop, and beyond, usually follow suit. Sometimes, the performance goes on for so long and involves so many monkeys that it is difficult to track who is displaying, and who isn’t.

Males respond to these signals by running after a displaying female, inspecting her swelling, chasing one after another, sometimes stopping to mount, sometimes not. Each female’s energetically expensive display may well function to increase access to several males, thereby allowing her to observe subtle aggressive and cooperative interactions between males.

One rainy morning, a female, which I had named Metoo, didn’t move out with the rest of the troop. Instead, she, her 18-month-old son, Mimp, and Mr. Mean, the number two male in the troop, waited until the others had headed for the raphia palm swamp and were out of sight. The three then headed in the opposite direction toward the woodland-savanna.

For the next day and a half, the three rested, groomed, ate, slept, and the two adults mated repeatedly, out of sight of the troop. They didn’t make noise. They didn’t respond to calls. Clearly, they didn’t want other members to know where they were.

This tryst was not a first for Metoo and Mr. Mean. About two years earlier, before Mimp was born, Metoo had an infant that died. Mr. Mean spent two days sitting by Metoo’s side as she stayed with her dead infant. Neither adult made any attempt to follow, or join, other troop members during this period. Perhaps, Mr. Mean was anticipating Metoo’s departure from the troop or the resumption of her sexual cycle—both of which are related to the loss of an infant.

The dominant female with a full swelling rests with a mother and two of her three offspring.

Although overt sexual activity is the norm among red colobus monkeys in the Abuko Nature Reserve, especially during the mating season, the behavior of Metoo and Mr. Mean was not an isolated incident. Other rendezvous have been observed often enough in this forest and in other western red colobus populations to be normal behavior throughout the range.

The two males that I had observed taking part in trysts in the Abuko National Reserve were not dominant males. Neither of them was the preferred partner of most of the females in their troop. When they did attempt to mate, they were harassed by the dominant male. They were, however, the preferred sexual partner of their tryst partner. By quietly following a female away from the troop, they were free to engage in sexual activity uninterrupted. Conversely, most females that I studied opted to mate within the confines of the social unit. These females, however, did not mate indiscriminately. They didn’t pick the largest male. The dominant male, Captain Crook, was much smaller than Mr. Mean. In a species such as the western red colobus, where most males and females have a similar body size, females don’t need the extra protection afforded by an appreciably bigger mate. They also don’t choose the oldest male. Rather, they consistently choose the youngest available mate, selecting him even above the most sexually competent male. Captain Crook, for example, had a deformed penis and could not mate properly. Yet, the females did not seem to mind. Despite his inability to achieve intromission, they consistently chose him over Mr. Mean, who was more than competent. So, what qualities were they looking for?

They seem to have chosen the most persistent male. The first choice with females when in a fully swollen state was also the one they mated most with in all other states. If females prefer a male that is constantly attentive, then the energy and time a male spends pursuing, mounting, and resting with a female, when she is not yet ready to conceive, is not wasted. From the male’s point of view, it may be a long-term strategy.

Battle-scarred Captain Crook was the dominant male, being the preferred sexual partner, for a short reign before being replaced by a younger male.

The most persistent male was also the one with the highest status, which is defined as being the recipient of the least amount of aggression, while dispensing the most aggression toward other males. If dominance is important in mate choice, what does a female gain by mating with the dominant male? A short-term benefit is a peaceful coupling as the dominant male is not usually interrupted by other adult males. From a long-term perspective, it is difficult to see what advantage a female gains. A male’s career as chief copulator is very brief—usually just one mating season—so offspring do not benefit much past the first few months in paternal care and protection from the assumed father’s high status.

A mother and her large infant son who, when he grew up, deposed Captain Crook and became the dominant male and chief copulator.

But for colobus infants, those early days are a time of probable infanticide by males from outside the troop. During this period, new mothers seek out resident adult males more often after they give birth than before, and the male chosen is usually of the highest status. Mothers also “introduce” their newborns to the dominant male by running up with their infants ventrally presented, open-mouth kissing the male. So, it seems possible that infants might receive some extra protection during this vulnerable time. However, in the two instances that I observed alien males attempting to join a troop, they were immediately jumped on by females with an assisting male and literally ripped apart. Since the attacks were initiated by the females, with a male joining later, females and their young may not have needed a male’s protection.

On a longer-term basis, a female may choose to mate with the dominant male because he can pass his leadership qualities on to her offspring. There is, however, no firm evidence that female primates choose males on this basis or that the ability to achieve the highest rank is genetic.

Although not clear why females choose some males over others as sexual partners, their sexual behavior influences male–male interactions. Their loud screams, known as quavers, and their noticeable courtship displays cause males to compete with one another for sexual favors.

A young female displays a full threat face and exhibits the very beginning of her first sexual swelling.

Interestingly, females who went on secret assignations didn’t give copulation quavers or courtship displays when they were with their preferred mates. However, as they rejoined their troop, they immediately announced their presence by quavering and displaying.

So, what can we conclude? It would appear that males, depending on their ranking, have two separate strategies to mate and spread their genes to the next generation. The dominant male mates with females within the confines of the troop, whereas lower-ranking males may leave the troop to mate uninterrupted. It appears that females who favor the non-dominant males understand this and lead them away from potential harassment.

An adolescent female from a neighboring troop spies on the focal troop. She, and a few of her age mates, eventually left their natal troop and became fully fledged members of the focal troop where they mated, gave birth, and raised their young.

These patterns of sexual behavior must be viewed in conjunction with the fact that females not only select some males and reject others, they also choose to join specific troops and then play a large role in determining who will and will not be accepted into their troop.

Over the years of study of western red colobus in Abuko, females have demonstrated that they are not shy, passive or subordinate to a male “warlord.” In their youth, they display curiosity and a tendency to leave their home troop usually with age-mates for new and different experiences. As adults, they are assertive within their troop and fierce fighters, often chasing away strangers from their home range, staunchly defending their young against any who dare to make them squeal, and sometimes even initiating fatal attacks against intruder males.

For a few months every year, the forest is taken over by females acting with sexual abandon. While sex is not the only component of the lives of these red colobus females—they are also friends, mothers, sisters, and daughters—the outcome of these highly charged few weeks has profound implications for their future reproductive success.

ALL IS NOT WELL

Habitat destruction is one of the most serious threats to primates worldwide. The Gambia, the smallest and most densely populated country on the African mainland, is no exception. Inappropriate land-use practices, uncontrolled bush fires, overgrazing by an increasing stock of domestic animals, soil degradation and erosion, and improper natural resource management all combine to form a spiral of habitat decline. The results of all this have led to small, discrete patches of forest surrounded by land that is unsuitable for red colobus monkeys.

While the endangered red colobus monkeys congregate in low densities throughout The Gambia, within highly fragmented, small forested areas such as the Abuko Nature Reserve and the Bijilo Forest Park on the Atlantic Coast, they are also now found in extremely dense populations. From 1983 to 2005, the colobus population in Abuko jumped from 132 individuals inhabiting five separate troops to about 220 individuals inhabiting six troops. During the same time span, the Bijilo population jumped from about 35 individuals in two troops to 100 individuals inhabiting three troops. These high population numbers in these fragmented forests do not mean all is well. Rather, they are cause for concern. Since small, unprotected patches of forest in The Gambia disappeared and were turned into agricultural fields, residential areas, and tourist enclaves, habitat degradation outside Abuko and Bijilo may be the cause of elevated monkey densities inside the forested areas. Colobus are probably emigrating from other areas into Abuko and Bijilo. In order to do that, they travel through what is undoubtedly unsuitable and probably quite unsafe colobus habitat. —DS 

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Some red colobus monkeys in estrus are uninhibited,  unintimidated, and unconventional in their mate choices.