Mandrillus Sphinx- Sexual Dimorphism And Physical Diversity Of Individuals In Relation To Social Status

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Mandrillus sphinx: Sexual Dimorphism and Physical Diversity of Individuals in Relation to Social Status A case study by Jonathan Schwartz November 8, 2006 Biological Anthropology and Anatomy 143: Primate Ecology Duke University

2 Within the order Primates is a magnificently diverse range of species; in taxonomy, geographical range, and lifestyle. This much is immediately obvious even from distant, secondhand study of primates. It is also paramount, however, to recognize that this variation is not limited to species by any means, and that it extends to the individual. Social roles- in some species more so than others- do much to dictate individual animals’ behaviors and physical appearances. Some prominent and widespread categories of these diverse roles stem from gender, as well as social status (particularly the dominance rank among males). Many primate species would be effective case studies for these phenomena of intraspecific diversity, but in this specific study, Mandrillus sphinx will be examined in detail and depth on the grounds that it is a particularly exemplary species for this topic. Mandrillus sphinx (common name: mandrill) is an Old World monkey (Superfamily Cercopithecoidea)1 native to West Africa. It is often informally referred to as a baboon, and while it is true that taxonomists once classified mandrills in the Papio genus (the genus containing all baboons), mandrills have since been given their own genus of Mandrillus by Groves in 1989 (“Mandrillus sphinx”). They share this genus with only one other species: the highly endangered Mandrillus leucophaeus (common name: drill). The name “mandrill” literally means “man-like drill,” with “drill” of course simply referring to its nearest relative, which is an old West African name for the monkeys (“America Zoo”). Drills have had their native home range in Cameroon and southeastern Nigeria almost completely depleted by human development, and have consequently had their range almost entirely confined to the island of Bioko, which belongs to the small West African nation of Equatorial Guinea. Drills were, in fact, rated by the International Union for Conservation of Nature and Natural Resources (IUCN) as the highest conservation priority among all African primates (Massicot 1

See (Fig. 1) for full taxonomy.

3 2006). The mandrill’s geographical range is quite broad compared to those of its more endangered cousins, but still rather small compared to many primate species, straddling the equator and confined roughly between the latitudes of 4°N and 4°S. Its western boundary is the Atlantic Ocean, but the full extent of its eastern range is still ambiguous. Wild mandrills live primarily within the borders of Gabon, Equatorial Guinea, and southern Cameroon (south of the Sanaga River); although occasionally they have also been sighted in isolated regions of the Republic of the Congo (“Mandrillus sphinx”)2. The mandrill is a uniquely distinctive animal. It is the largest monkey in the world3, (Feistner 2005) usually measuring from 61-76cm in length and up to 80cm tall. Females weigh an average of 11.5kg, but males weigh an average of 25kg. Some of the largest males have been known to weigh up to 54kg. It is evident from this basic data that a great deal of sexual dimorphism exists within the M. sphinx species; however, as it turns out, the dimorphism extends beyond a difference in size. Perhaps the mandrill’s most recognizable feature is its bright colors: this includes a red stripe down the center of the face, and light blue ridged segments on either side of the stripe. The fur is olive-colored, the rump is bright blue, and a yellow-colored beard hangs from the chin. These colors are far more pronounced in mature males than in females or juveniles (Ingmarsson 1999). The physical distinctions between sexes, as well as the distinction between males of different social rank, will be discussed in depth later in this paper. The mandrill’s morphology allows for a diverse range of easy locomotion. Unlike most monkeys, it has adapted to a primarily terrestrial lifestyle as opposed to an arboreal one, although it does often shelter itself in trees at night. The combination of strong, long limbs, a 2

See (Fig. 2) for map of range. This includes both Platyrrhini and Catarrhini infraorders, with “monkey” defined as any non-hominoid anthropoid. 3

4 clavicle, and opposable thumbs allow it to climb trees with ease while also maintaining a natural quadrupedal walk, which allows for their terrestrial daytime lifestyle. Their tails are considerably shorter than those of most monkeys, which indicates less reliance on treeclimbing4. Like most primates, they are native and best adapted to tropical rain forest habitats (Ingmarsson 1999). Like all Cercopithecines, mandrills are largely frugivorous and contribute to seed dispersal in forests (Ingmarsson 1999). However, they have been known to supplement their diet with a variety of other foods. Various researchers have observed mandrills for lengthy periods of time and collected fecal samples to estimate the relative amounts of different types of food the mandrill consumes, and the results of this research has varied some depending on the location, most likely due to differing abundances of specific food resources. Specifically, one study in the Lope Reserve in Gabon (Tutin et. al. 1997) yielded a higher percentage of leaves (8.2%) than a study in Cameroon conducted by Hoshino (1985), while the Cameroon study yielded a higher percentage of animals (7.6% vs. 4.1% in Gabon). Both studies, however, revealed that mandrills have a dietary staple of about 84% fruit or fruit material5 (Flannery 2003). It is not known why mandrills consume this specific amount of fruit and supplement the remainder of their diet with leaves, animals, fungi, and even small amounts of soil, but it is a trend that is not uncommon among primates. Mandrills, however, are able to eat more animals than most other monkeys due to their large size. Animals that serve as prey for mandrills include insects, worms, snails, frogs, lizards, and on some occasions they have even been observed to eat snakes (Ingmarsson 1999). Still, perhaps the mandrill’s most impressive hunting feat is the predation of Cephalophus dorsalis, or duiker, a small African 4

Many monkeys use their tails for balance or grasping branches. Both functions enable a highly arboreal lifestyle. When mandrills do need to climb trees, they utilize their opposable thumbs. 5 Includes seeds and pith.

5 antelope species (Kudo & Mitani, 1985). Predation of such large vertebrates is not common and has only been observed on isolated occasions. Another unique dietary trait of the mandrill is that, due to its terrestrial lifestyle, it mainly eats fruit that has fallen off the tree already. Some have speculated that this accounts for why the mandrill has a large home range when compared to other primate species in similar environments (Hoshino et al., 1984). It is not entirely known whether mandrills have any significant predators, but some evidence indicates that Panthera pardus (leopards) might prey on mandrills. This evidence comes from analysis of leopard feces, although it remains possible that the leopard was merely scavenging and consumed some mandrill carrion. The mandrill, though not technically endangered like its previously discussed relative, the drill, is classified as “vulnerable,” which means that it is at risk of becoming endangered. In recent years the mandrill has suffered a population decline, primarily due to habitat destruction by humans. A more minor, but not insignificant problem that humans have caused for the mandrill is from hunting. Mandrills are sometimes locally hunted for food. Because of their loud vocalizations, they often make themselves conspicuous to these hunters. Additionally, mandrills have a reputation as pests to some West African farmers. As a result of too much habitat destruction, mandrills are occasionally forced to “steal” crops. This unfavorable reputation may contribute to a harmful lack of effort to preserve the species (Ingmarsson 1999). Mandrills are known to be an exceptionally gregarious species. A common social organization of mandrills is a harem structure, in which there is a single large, dominant male who is polygynous. The male has exclusive mating rights over the females who make up the remainder of the group, and these groups have been known to contain up to 15 individuals.

6 However, sometimes mandrills are found in extremely large groups, ranging up to several hundred individuals. These groups consist of many males and many females. Breeding is infrequent, occurring only about once every two years, and females typically give birth to only one offspring at a time. Mating season is in the summer, and the gestation period lasts 220 days. Mandrills may live up to 46 years (“Mandrill” (BBC)). The intricacies of the mandrill social structure will be under close examination for the remainder of this paper. Specifically, the process under which a male may rise to dominance will be investigated, as will the events that occur to those males that never do become harem leaders. The sexually dimorphic nature of mandrills, which are believed to have more sexual dimorphism than any other primate species (Charpentier et al. 2004), is not to be overlooked when investigating these subjects and it in fact will be another main focal point of this case study. The relationship, if any, between the male dominance in this species and the extreme dimorphism will be taken into close consideration. Juvenile males have yet to grow to the comparatively huge size of their adult counterparts, nor have they yet acquired the colors. Therefore, it is apparent why the adolescent life stage for males would be of great interest. Charpentier et. al. explore this realm in a 2004 experiment involving the social interactions of eleven adolescent males. As the researchers mention, mandrills are a good choice for an experiment such as this because the adolescent phase is very long, lasting from approximately four to ten years of age. During this time, male mandrills undergo major growth spurts, and the colors on the face, rump, and genitalia all brighten. Charpentier et al. observed that among the 11 adolescents, the eight younger individuals formed a cohort, while the other three were more solitary and more aggressive. Female adolescence lacks this long, eventful phase, presumably because

7 they do not require nearly as much change from juvenile to adult. Female adolescents are in fact difficult to define in mandrills because so little change occurs, save for the obvious development of gametes. Due to this difficulty, the category of “female adolescents” was altogether omitted from the experiment. The experiment categorized types of behavior, which was recorded through close observation of all eleven individuals, scored against control groups involving every other gender/age combination, excepting the aforementioned female adolescents. Certainly the results showed that the rise to male dominance was as gradual and defined as physical development might indicate. One key lesson of the experiment is that “adolescent” is perhaps not a sufficient categorization for a mandrill between the ages of four and ten. The researchers found that two distinct levels of male mandrill adolescence exist. The first, exemplified by the cohort of eight younger individuals, begins around the age of four, when the testicles descend. This life stage is categorized by mainly conspecific interaction among others in the same age group, including a heavy emphasis on playing. Once the mandrills age past that stage, however, they begin to engage in primarily aggressive interaction towards virtually every other group, with the notable exception, unsurprisingly, of adult males. This was exemplified by the three older adolescents not included in the previous cohort. Adult males, however, as seen in Charpentier et al. (2004, p. 70), exert by far the smallest amount of aggression on other group members despite receiving the bulk of it. Perhaps it is safe to assume that this is due to his duty as the protector of the group, or harem, if applicable. This leads to the realization that because of their unrivaled combination of strength and aggression, older male adolescents are by far the most dangerous members of the group, and in general the most dangerous mandrills toward other mandrills. It is

8 interesting to speculate on the reasons for this, but one possibility is that it serves as a tactic to gain acceptance. Male adolescents vie for dominance, and gain the respect of fellow group members through aggressive behavior. The issue of dominance among wild mandrill groups will be discussed further in subsequent studies, which will be carefully analyzed. Although Charpentier et al.’s study brought to light some informative data about the details of male mandrills’ growth and development, one factor in their study was largely ignored- social rank. Setchell and Dixson (2002) also observe the male mandrill’s growth in the adolescent phase, but they concentrate on the mandrills’ relative social status. It was observed that the males that rose to dominance and were more social had larger testes and higher testosterone levels, while the males that were more “peripheral and solitary” (Setchell & Dixson 2002, p. 9) had smaller testes and lower testosterone levels. The study measured 13 males aged five to nine years at the International Medical Research Center in Gabon over a 21-month period (Setchell & Dixson 2002, p. 10), and measured various characteristics in these males and the degree to which they changed over time. These traits included, among others, body mass, testosterone levels, the brightness of the male sexual colors on various parts of the body, and the age at which they left their natal groups. Setchell and Dixson ultimately concluded that “Marked individual differences in the timing of testicular function, sexual skin coloration, and other features are also apparent in males, as well as differences in the ages at which they emigrate from their natal groups. These differences correlate most strongly with male dominance rank, so that high-ranking males develop faster and emigrate earlier than subordinate males in mandrill social groups (Setchell & Dixson 2002, p. 23). This data may seem unsurprising, considering that the traits most unique to males were more pronounced in the males that rose to dominance in the social structure. It seems

9 clear that there is a genetic component to the factors that determine male dominance. However, Charpentier et al.’s study, discussed earlier, revealed that essentially all adolescent males go through a solitary and sometimes aggressive phase, usually between their sixth and tenth years of age. Since this phase is virtually universal among male mandrills, it would seem to suggest that all male mandrills make an attempt to rise to dominance. The purpose of the solitary phase in adolescents is thought to be for males to develop better survival skills, which they would need in adulthood especially if they were to become dominant males over a harem. As mentioned earlier, a harem structure consists of one dominant male and up to fifteen females with whom he has exclusive mating rights. Common sense regarding simple gender ratios should tell us that it is not possible for all males to rise to this level of dominance. Therefore, it is reasonable to assume that a certain degree of intraspecific competition is present among males approaching adulthood, mostly over mating prospects. In summation, it appears likely that male dominance is determined by both genetics and by competition. Two reasonable questions that may now be asked are simply; why do mandrills have this male-dominant harem structure, and why do they exhibit such extreme sexual dimorphism? It is easy to answer these questions one at a time with the assumption that the other condition is already in place. For instance, it is not difficult to imagine why males having a much greater body size than females might make them more dominant, and it is easy to see why a harem structure works better when this natural sign of dominance exists. However, the question becomes much more difficult if neither sexual dimorphism nor the harem social structure is assumed to have previously existed. What might cause these elements of mandrills’ genders and lifestyles to evolve?

10 Firstly, it is important that mandrills’ sexual dimorphism with regard to body size is not unique among Cercopithecines. For examples, males may be up to twice the size of females in Papio hamadryas, and the males also have a large, bushy mane that the females lack (“Hamadryas baboon, sacred baboon” (BBC)). In fact, all baboons are dimorphic in size. Mandrills were thought for a long time to be baboons (members of the Papio genus), but were separated from them recently. Nonetheless, they continue to share many characteristics with them. It turns out that Papio hamadryas baboons also share the mandrill’s harem social structure. Now it is evident that the concurrence of sexual dimorphism and male-dominated social structures may be a trend among some monkeys. Perhaps a logical reason for these phenomena concurring in many Cercopithecines lies within their life histories. It was previously mentioned that mandrill females typically give birth to only one offspring at a time, yet their gestation periods are fairly long and females only mate approximately every two years. This may be a legitimate reason for the harem structure. Normally, such statistics would be foretelling of a low birth rate, which could lead to population declines6. Harem structures, however, by making a single male readily available to all females in mating season, would allow females to reproduce as often as they are ready. It also ensures no shortage of females to the most dominant males. This explanation for harem structures in mandrills would make it clear why sexual dimorphism in body size is necessary. It ensures male dominance within these harem structures and allows a maximum number of total offspring to be produced for group. It also eliminates the element of competition for mates within groups, although males may still possibly compete for social status during their adolescent years, as mentioned before. Even 6

It was previously mentioned that mandrill population is suffering a decline. This is due mostly to human activities including hunting and land development. Mandrills could be especially susceptible to this because they have very few natural predators and may be unaccustomed to hiding or defending themselves.

11 under this hypothesis, ambiguities abound. For instance, Setchell et al. (2006) recently observed an event that raises some questions about the degree to which male dominance is absolute. Setchell et al. chronicle the observation of several female mandrills attacking a dominant male who had been injured by another male. Also mentioned in their report was that in previous observations, large groups of female individuals had even been reported to kill a male (Setchell et al. 2006, p. 411). The researchers concluded that this observation “suggests that females have a degree of control over male group membership, despite the large degree of sexual dimorphism in this species” (Setchell et al. 2006, p. 411). These isolated incidents are puzzling given what we know about sexual dimorphism’s contribution to male dominance. Another element of sexual dimorphism that remains unexplained is arguably the mandrill’s most defining feature- the bright colors that appear on the male during puberty. The presence of these colors is what most notably distinguishes the mandrill from its closest relative, Mandrillus leucophaeus, or the drill. As reported earlier, the brightness of these colors correlates to dominance. Darwin, in fact, used the mandrill as an example for his theory of sexual selection, and studies have indicated that females do indeed usually prefer brightly colored males. If the mandrill and the drill diverged from a common ancestor, it is reasonable to ask what prompted the development of the mandrill’s bright colors, and whether they have anything to do with the mandrill’s superior success at survival than drills, which are among the world’s most endangered primate species. Andreas Paul (2001) explored this unanswered question of evolution. Although no conclusion has been reached, Paul offers some theories as to how the change may have come about. Paul states that Darwin’s theory that females prefer brightly colored males is “unproven,” but states an

12 alternative explanation made by Wickler in 1967, in which Wickler hypothesized that the function of the colors was instead to have a “’demoralizing effect’ on possible rivals” (Wickler 1967, p. 120) (Paul 2001, p. 897). If Wickler’s hypothesis is accurate, brightly colored males would still have a greater chance of mating because they would have the advantage in competition with other malesnot because of sexual selection. If Darwin’s theory of sexual selection applies to the mandrill, then evolution is seemingly more complicated, because not only would males have to evolve the colors, but females would have to evolve a preference for the colors. This seems illogical if the colors did not yet widely exist around the time when mandrills diverged from drills. Wickler’s hypothesis seems more likely, only because it requires a single evolutionary event in males which the females would subsequently evolve to adapt to, as opposed to Darwin’s theory in which male and female change would be mutually dependent upon one another. Some researchers including Setchell and Dixson have documented an apparent higher likelihood of reproductive success for brightly colored males, but to determine the cause of this success would be far more difficult. Perhaps someday an experiment could be arranged to determine the nature of this remarkable phenomenon unique to Mandrillus sphinx.

Literature cited “America Zoo” (On-line). Accessed November 06, 2006 at http://www.americazoo.com/goto/index/mammals/111.htm. Charpentier, M., Peignot, P., Hossaert-McKey, M., and Wickings, E.J. 2004. Changes in Social Interactions During Adolescence in Male Mandrills (Mandrillus sphinx). American Journal of Primatology. Vol. 63(2), 63-73.

13 Feistner, Dr. Anna. April 02 2005. “Mandrill- Mandrillus sphinx” (On-line), ARKive. Accessed November 06, 2006 at http://www.arkive.org/species/GES/mammals/Mandrillus_sphinx/. Flannery, Sean. October 09, 2003. “Mandrill- Mandrillus sphinx” (On-line). Accessed November 06, 2006 at http://members.tripod.com/uakari/mandrillus_sphinx.html. “Hamadryas baboon, sacred baboon” (On-line). Accessed November 08 at http://www.bbc.co.uk/nature/wildfacts/factfiles/228.shtml. Hoshino, J. 1985. Feeding ecology of mandrills (Mandrillus sphinx) in Campo Animal Reserve, Cameroon. Primates. Vol. 26(3), 248-273. Ingmarsson, L. 1999. "Mandrillus sphinx" (On-line), Animal Diversity Web. Accessed November 01, 2006 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Mandrillus_sphinx.html. Kudo, Hiroko, and Matani, Masazumi 1985. New record of predatory behavior by the mandrill in Cameroon. Primates. Vol. 26(2), 161-167. “Mandrill” (On-line). Accessed November 01 at http://www.bbc.co.uk/nature/wildfacts/factfiles/232.shtml. “Mandrillus sphinx” (On-line). Accessed November 01 at http://www.gisbau.uniroma1.it/amd/amd081.html. Massicot, Paul. August 01 2006. “Animal Info- Drill” (On-line), Animal Info. Accessed November 01, 2006 at http://www.animalinfo.org/species/primate/papileuc.htm. Paul, Andreas. 2002. Sexual Selection and Mate Choice. International Journal of Primatology. Vol. 23(4), 877-904. Setchell, Joanna M., and Dixson, Alan F. 2002. Developmental Variables and Dominance Rank in Adolescent Male Mandrills (Mandrillus sphinx). American Journal of Primatology. Vol. 56(1), 9-25. Setchell, Joanna M., Knapp, Leslie A., Wickings, E. Jean. 2006. Violent coalitionary attack by female mandrills against an injured alpha male. American Journal of Primatology. Vol. 68(4), 411-418, Tutin, C.E.G., Ham, R.M., White, L.J.T., and Harrison, M.J.S. 1997. The primate communtiy of the Lope Reserve, Gabon: Diets, responses to fruit scarcity, and effects on biomass. American Journal of Primatology. Vol. 42, 1-24. Wickler, W. 1967. Socio-sexual signals and their intra-specific imitation among primates. In Morris, D. (ed.), Primate Ethology,Weidenfield and Nicholson, London, pp. 69–147.

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Figure 1: Taxonomy of Mandrill

Order Primates Suborder Anthropoidea Infraorder Catarrhini Superfamily Cercopithecoidea Family Cercopithecidae Subfamily Cercopithecinae Genus Mandrillus Species sphinx