Animal Diversity Web

Geographic Range

Piliocolobus kirkii, the Zanzibar red colobus, is endemic to the Unguja, Uzi, and Vundwe Islands of the Zanzibar archipelago off the coast of mainland Tanzania. Unguja island is home to the largest population of P. kirkii, but the species has a highly fragmented distribution and is limited to remnant pockets of forest in the east, south-central, and southeast portions of the island, including Jozani Chwaka Bay National Park, Makunduchi, Muongoni, Kiwengwa, and Popakani (Silkiluwasha 1981; Struhsaker 2010). A small population of 14 individuals was reintroduced into Ngezi forest on Pemba Island in 1974, where some red colobus monkeys may still persist, but the size and viability of the current population is unknown (Struhsaker and Siex 1998; Campero Ciani et al. 2001). (Campero Ciani, et al., 2001; Silkiluwasha, 1981; Struhsaker and Siex, 1998; Struhsaker, 2010)

• Biogeographic Regions
• ethiopian
  • native

• Other Geographic Terms
• island endemic

Habitat

Zanzibar red colobuses inhabit coral-rag scrub forest and mangrove swamps. In Jozani National Park, several populations also inhabit bordering farmland - known as “shamba” in Kiswahili - that is characterized by a mixture of perennial agriculture, exotic trees, and scrub forest (Siex and Struhsaker 1999b; Struhsaker 2010). On Uzi Island, disturbance of the coral-rag forest has led to compression of tred colobus populations in mangrove forest refugia. Though some groups on Uzi Island spend upwards of 85% of their time in mangrove habitat, it is unlikely that the mangrove refugia alone – without access to adjacent coral-rag thicket – would support viable populations of these monkeys (Nowak 2008). Mangroves are used as a refuge from human disturbance and as a reliable source of shelter, but it is thought that the mangrove diet may not be sufficient to sustain these monkeys, as more time is spent feeding on preferred food sources in coral-rag forest (Nowak 2008). (Nowak, 2008; Siex and Struhsaker, 1999a; Struhsaker, 2010)

• Habitat Regions
• tropical
• terrestrial

• Terrestrial Biomes
• forest
• scrub forest

• Other Habitat Features
• agricultural
• riparian
• estuarine

• Average elevation

  2 m

  6.56 ft

Physical Description

Like other red colobus species, P. kirkii is a medium-sized monkey with a distinct build. It has a small head on a long-backed, pot-bellied body and very long limbs - with the hind limbs being slightly longer than the forelimbs (Kingdon 1997). All colobine monkeys share several features, including a greatly reduced thumb, a long tail, and elongated hindfeet (Struhsaker 2010). Red colobus species (Piliocolobus) differ from black-and-white colobus species (Colobus) in having a much smaller larynx and no subhyoid sac. Other defining features are the separated ischial callosities of males and the presence of perineal organs in males and females (Kingdon 1997). Adult and subadult females have true perineal swellings that vary in size over the estrus period but are consistently smaller in P. kirkii than in other red colobus species (Struhsaker and Leland 1980; Struhsaker 2010). Young males also have a perineal organ - a small protuberance around the anus that superficially resembles a small swelling – that is retained in adult males, though in a reduced form (Struhsaker and Leland 1980). Zanzibar red colobuses are the smallest Piliocolobus species (Struhsaker 2010).

Zanzibar red colobuses have distinctive pelage with red, black, and white regions (Kingdon 1997). The upper back and shoulders are black and the middle and lower back varies from orange to red-brown. There is pronounced individual variation in the extent of black and red-brown on the nape, shoulders, and upper back. The anterior edge of the shoulders, the ventral area, and the medial surface of the arms and legs are white to grey. The ventral surface of the tail is white or grey mixed with blonde hairs, the dorsal surface is red-brown with the distal half sometimes blending into blonde. The legs are grey, except for a black stripe on the lateral thigh. The lateral surface of the forearms is mostly black but varies in the amount of additional white or grey. The dorsal surfaces of the hands and feet are black (Struhsaker and Leland 1980; Kingdon 1997; Struhsaker 2010).

The black face is framed by a fringe of long white hair that extends to the red-brown crown of the head. The lips and noses of infants are pink, but vary significantly between pink and black in adults within the same social groups (Struhsaker 2010). The natal coat color of infants is black and white. The characteristic red and brown colors do not appear in infants until they are 3 to 5 months old and full adult coloration is achieved between 6 and 11 months of age (Nowak and Lee 2011a).

There is less sexual dimorphism in body size in P. kirkii than in other Piliocolobus species, with an average body weight of 5.8 kg for males and 5.5 kg for females (Struhsaker 2010). Sexual dimorphism is pronounced in cranial dimensions and canine length, however. Adult males have much longer canines, a more robust skull, and a well-developed nuchal and sagittal crests. The tail of males is generally thicker and more heavily furred than those of females. In contrast to other Piliocolobus species, adult females have significantly longer bodies and tails than dp adult males (Struhsaker 2010). (Kingdon, 1997; Nowak and Lee, 2011a; Struhsaker and Leland, 1980; Struhsaker, 2010)

• Other Physical Features
• endothermic
• homoiothermic
• bilateral symmetry

• Sexual Dimorphism
• male larger
• sexes shaped differently

• Average mass

  5.5 (females) - 5.8 (males) kg

  lb

• Range length

  45 to 70 cm

  17.72 to 27.56 in

• Average length

  55.4 cm

  21.81 in

Reproduction

Zanzibar red colobuses are promiscuous and copulation is initiated by both sexes. Females often copulate with more than one male during a given estrous period (Struhsaker 2010). In a long-term study of P. kirkii in Jozani forest, all copulations observed were between members of the same social group (Siex 2003; Struhsaker 2010). Zanzibar red colobuses are multiple mounters, meaning that one or more incomplete mounts precede the mount during which ejaculation occurs. During a mount, the male delivers pelvic thrusts and then pauses when ejaculation occurs. In contrast to most cercopithecids - in which the male’s hindfeet grip the female’s calves during copulation - in P. kirkii, the male’s hindfeet remain on the substrate. Females have sometimes been seen to shudder and vocalize during or following copulation. Copulating pairs are harassed by other group members - usually adult males and juveniles. Harassment of the copulating pair occurs in a variety of ways, including leaping around the pair; grabbing, slapping, and twisting of the male’s head; and climbing onto the male. Harassment by adult males is likely a form of intrasexual competition, whereas harassment instigated by juveniles may represent parent-offspring conflict (Struhsaker 2010). (Siex, 2003; Struhsaker, 2010)

• Mating System
• polygynandrous (promiscuous)

Both sexes disperse from natal groups before any sexual activity occurs - often at an age of 37 to 52 months. Juveniles integrate into new groups before reproductive activity is initiated (Siex 2003). The age for the onset of reproductive activity has not been described in P. kirkii, but is 53 to 59 months in Piliocolobus tephrosceles and full reproductive maturity is reached after 60 months in Piliocolobus tephrosceles . In P. kirkii, females reach sexual maturity somewhat earlier than males and full reproductive maturity is attained at an estimated 4 to 5 years for females and 5 years for males (Struhsaker 2010). Zanzibar red colobuses do not have a distinct breeding season and copulations and births occur throughout the year – though births peak in distinct seasonal periods that vary somewhat between sites. In Uzi and Vundwe, most births occur during the wet season (October-December), whereas in Kiwengwa, births peak during the dry season (January-February) (Nowak and Lee 2011a). Females typically give birth to one young, though occasional twin births have been reported (Struhsaker 2010). Based on extrapolation from other Piliocolobus species, one estimate of the typical length of interbirth intervals in P. kirkii is 24 to 30 months. Another estimate based on studies of the Uzi, Vundwe, and Kiwengwa populations of the Zanzibar Red Colobus places the interbirth interval length at 28 to 36 months (Nowak and Lee 2011a).

There is evidence for paternity confusion strategies in females of Piliocolobus tephrosceles. In P. tephrosceles, female swellings are highly variable, last for long periods of time, and occur during pregnancy as well as in regular estrus cycles. Consequently, swelling size is an unreliable indicator of female sexual receptivity, and may thus hold great potential for paternity deception. Reports of infanticide by male P. kirkii has led some to speculate that Zanzibar red colobuses may employ similar paternity deception strategies (Struhsaker 2010). (Nowak and Lee, 2011a; Siex, 2003; Struhsaker, 2010)

• Key Reproductive Features
• iteroparous
• year-round breeding
• gonochoric/gonochoristic/dioecious (sexes separate)
• sexual
• viviparous

• Breeding interval

  Breeding occurs throughout the year, but estimates of interbirth interval length range from 24 to 36 months.

• Breeding season

  Zanzibar red colobuses have no distinct breeding season.

• Average number of offspring

  1

• Average gestation period

  5-6 months

• Range weaning age

  12 to 36 months

• Range time to independence

  37 to 52 months

• Average age at sexual or reproductive maturity (female)

  4-5 years

• Average age at sexual or reproductive maturity (male)

  5 years

Young are altricial and weaning may not be complete until two years of age. Infants are carried, clinging to the belly of the mother, for 6 months. After that, infants can locomote independently but may continue to be carried by the mother for more than a year. Juveniles become relatively independent at the age of 24 to 36 months, when they are mainly self-sufficient and feed entirely on adult foods. Complete independence is achieved with dispersal from the natal group, which usually occurs at an age of 37 to 52 months (Nowak and Lee 2011a). Grooming of infants by non-mother females and allomothering (handling and carrying infants of other females) has only been reported in P. kirkii - not in any other Piliocolobus species. The degree and frequency of allomothering in P. kirkii is, however, much less than that seen in other Cercopithecidae species (Siex 2003; Struhsaker 2010). There is some evidence for differential investment by mothers in sons compared to daughters, as sons are often suckled longer than daughters. Adult males have also been observed to suckle. In other Piliocolobus species, mothers groom their sons more than their daughters and develop longer-term affiliative relationships with sons. It is suggested that mothers invest more in sons than daughters in order to increase their inclusive fitness (Struhsaker 2010). (Nowak and Lee, 2011a; Siex, 2003; Struhsaker, 2010)

• Parental Investment
• altricial
• female parental care
• pre-fertilization
  • provisioning
  • protecting
    • female
• pre-hatching/birth
  • provisioning
    • female
  • protecting
    • female
• pre-weaning/fledging
  • provisioning
    • female
  • protecting
    • female
• pre-independence
  • provisioning
    • female
  • protecting
    • female
• post-independence association with parents

Lifespan/Longevity

The longevity of Zanzibar red colobuses is not known. Ugandan red colobuses (Piliocolobus tephrosceles) may live up to 21.2 years for females and 15.5 years for males in the wild. The mean lifespan for P. tephrosceles in the wild is 13.7 years for females and 10.5 years for males (Struhsaker 2010). Two other Piliocolobus species, Temminck’s red colobuses (Piliocolobus temminckii) and the Tana River Red Colobus (Piliocolobus rufomitratus), are known to live at least seven to eight years (Struhsaker 2010).

The Zanzibar Red Colobus has never been held successfully in captivity. An animal held at Antwerp Zoo in Belgium in 1964-1965 survived in captivity the longest, but this was not more than seven months (Gijzen et al. 1966). (Gijzen, et al., 1966; Struhsaker, 2010)

Behavior

Zanzibar red colobuses are social, living in multimale, multifemale social groups that usually contain two or more adult males. The average adult sex ratio (female/male) measured for Jozani populations is high and more variable than other Piliocolobus species, with a mean of 4.6 females for every male (range 2.4 to 13.7) (Siex 2003). This compares to a mean ranging between 1.6 and 4.1 females per male in other Piliocolobus species (Struhsaker 2010). The high variability in sex ratio of Jozani populations is likely a result of habitat compression of social groups into areas of forest edge and shamba farmland due to human destruction of their nearby habitat. This process resulted in high immigration rates, particularly of males, into existing shamba farmland groups (Siex 2003; Siex and Struhsaker 1999b). Only males establish dominance hierarchies, which is expressed by supplantation over space or food. Two forms of social presenting are related to male dominance: submissive presenting by adult females and juveniles to adult males, and another form of presenting in which dominant males show their backsides mainly to subordinate males, apparently to reinforce dominance hierarchies (Struhsaker 2010). Zanzibar red colobus societies are further characterized by fission-fusion, in which socially integrated groups regularly divide into temporary subgroups of smaller foraging units (Estes 1991). This fission-fusion social system seems to be related to food availability and distribution and is thought to be a way of integrating cost-effective foraging strategies with the social benefits of group living (Struhsaker 2010). Fission-fusion societies are found in other Piliocolobus species, but subgroups tend to be smaller in P. kirkii. This may be related to scarcity and seasonality of food availability, clumped distribution of food resources, and the absence of predators. Solitary males have also been observed in P. kirkii and are thought to represent dispersal and attempted immigration into new groups. The incidence of solitary behavior is higher in P. kirkii than in mainland Piliocolobus species. This is probably due to the absence of predators on the Zanzibar Islands (Siex 2003; Struhsaker 2010).

Some of the highest and most variable population densities of any non-human primate have been reported in Zanzibar red colobuses of Jozani National Park (Siex and Struhsaker 1999b). Highest population densities are reported for populations inhabiting shamba farmland bordering the park (4.5 times higher than in the coral-rag forest inside the park), where food trees occur in higher densities and are more uniformly dispersed than in the coral-rag forest (Siex and Struhsaker 1999b). As with other colobine species, population densities appear to be largely reliant on food density and quality (Siex 2003; Struhsaker 2010).

Activity budget analyses of Jozani forest and shamba farmland groups showed no difference in the time spent feeding or resting, but forest groups spent significantly more time moving and had longer daily travel distances (Siex 2003). Shamba farmland groups spent more time engaging in social behavior such as play, grooming, and aggression. These differences in activity budgets may be due to differences in the diversity of herbaceous food species available in each habitat. Herbaceous food species are more diverse in areas of shamba farmland and constitute a greater proportion of the diet than in forest groups (Siex 2003; Struhsaker 2010).

Aggression has been studied quite extensively in P. kirkii and in Piliocolobus monkeys more widely (Struhsaker 2010). In terms of intergroup relations, troops are generally tolerant of each other, but the rate of intergroup conflict increases with higher population density. Intergroup supplantations over food are relatively common in populations that inhabit shamba farmland and are exceptional in that both males and females of most age classes engage in aggressive group encounters, whereas only adult and subadult males are involved in aggression in other Piliocolobus species. This aggression is likely due to competition for food resulting from extremely high population density in the shamba farmland area (Siex and Struhsaker 1999b; Struhsaker 2010). An inter-taxon comparison suggests that the rate of intergroup conflict increases logarithmically in relation to population density. It is likely that once a population reaches a certain density in relation to carrying capacity, food competition and intergroup conflicts increase exponentially (Struhsaker 2010).

Intragroup aggression has also been studied in Zanzibar red colobuses. Adult males are the most common aggressors, with adult and subadult males being aggressive toward one another most frequently over both mates and food (Struhsaker 2010). Much of this aggression occurs during periods of transition in dominance rank. It has been hypothesized that the perineal organ of young males evolved as a mediator of sociality by providing a permanent attraction or appeasement to adult males and by inhibiting potential male aggression (Kingdon 1997; Struhsaker 2010). Rates of aggression with physical contact (such as biting and grabbing) are generally low, except in the high density populations inhabiting shamba farmland. In shamba farmland populations aggression occurs most often over food and involves both males and females, suggesting that food competition is relatively high (Siex and Struhsaker 1999b; Siex 2003; Struhsaker 2010).

Grooming behavior in Zanzibar red colobuses has been studied in some detail (Struhsaker 2010). Adult females do the majority of grooming, and adult males are groomed most often. Infants are rarely groomed, but adult females groom infants and juveniles more often than is seen in other Piliocolobus species. In contrast to other colobines, males have never been seen grooming each other. This absence of male grooming may be related to frequent transfer of males between social groups (Struhsaker 2010).

Play is primarily an activity of infants and juveniles. Studies of the Jozani populations show that infants and juveniles in shamba farmland groups play significantly more than those in the forest groups (Siex 2003). Play in the shamba groups may be facilitated by their shorter daily travel times, spatial cohesiveness, and tendency to spend more time on the ground than do the forest groups. The size of potential play groups may also be important (Struhsaker 2010). (Estes, 1991; Kingdon, 1997; Siex and Struhsaker, 1999a; Siex, 2003; Struhsaker, 2010)

• Key Behaviors
• arboreal
• scansorial
• diurnal
• motile
• sedentary
• territorial
• social
• dominance hierarchies

Home Range

There is significant variation in home range size of P. kirkii (Siex and Struhsaker 1999b). Home ranges vary in size between 0.5 and 8.8 ha for populations inhabiting different sites and habitats (Nowak and Lee 2011a). Habitat type and quality, rather than group size, appear to be the main determinants of home range size in P. kirkii (Struhsaker 2010). There is also extensive overlap in the home ranges of neighboring groups. In a study of several populations at different sites, mean percentage of home range overlap between groups varied between 6.9 and 42.9% (Nowak and Lee 2011a). (Nowak and Lee, 2011a; Siex and Struhsaker, 1999a; Struhsaker, 2010)

Communication and Perception

Zanzibar red colobus vocalizations and visual displays are designed for communication within large groups and for interactions at close range with neighboring troops (Estes 1991). As in other Piliocolobus species, adult male P. kirkii are the primary vocalizers and use three different distress, warning, and threat calls: bark, chist, and wheet (Struhsaker and Leland 1980; Struhsaker 1981). Adult male P. kirkii also give a complex long call that is unique among the Red Colobus monkeys. These long call bouts begin with one or more yelps, followed by a series of warbles and shrill squeals. The long call is expressed in dominance displays, indicating sexual interest in females, and initiating and coordinating group movements (Struhsaker 1981; Struhsaker 2010).

Adult females and juveniles also give various screams related to distress. Adult female P. kirkii appear to be more vocal when living under high population density conditions, and this is likely related to the greater degree of intra- and inter-group aggressive encounters in high density versus lower density populations (Struhsaker 2010).

Visual communication is also important in Red Colobus monkeys, and they are thought to have distinct facial features, hair color, postures, and movements for this purpose (Estes 1991). (Estes, 1991; Struhsaker and Leland, 1980; Struhsaker, 1981; Struhsaker, 2010)

• Communication Channels
• visual
• acoustic

• Perception Channels
• visual
• tactile
• acoustic
• chemical

Food Habits

Zanzibar red colobuses are primarily folivorous. Young leaves are consumed most often, constituting 31.1 to 60.7% of the diet in forest and shamba populations, respectively. Fruit with seeds constitutes 10 to 31.7% of the diet. The remainder of the diet consists of mature leaves, petioles, flowers, and flower buds (Struhsaker 2010). Zanzibar red colobuses feed almost exclusively on unripe fruit, in which seeds are softer and more digestible, suggesting that seeds also constitute an important part of the diet. The unripe-fruit-with-seed diet includes a wide range of plant families, but is dominated by the sycamore fig (Ficus sycomoros) in Jozani forest populations and by coconuts (Cocos nucifera) in shamba farmland populations (Struhsaker 2010). Other species commonly consumed by Jozani populations of P. kirkii include Eugenia malaccensis, Turea floribunda, Brideria micrantha, Albizia sp., and Fluergia sp. (Walz 2006). Zanzibar red colobus populations inhabiting mangrove forests on Uzi and Vundwe Islands most commonly feed on mangrove species such as Sonneratia alba, Avicennia marina, Rhizophora mucronata, Bruguiera gymnorhiza, and Ceriops tagal (Nowak 2008).

Like other colobines, P. kirkii is a foregut fermenter with a complex four-chambered stomach (Estes 1991). The stomach is divided into chambers wherein vegetation undergoes fermentation and predigestion by gut microflora before passage into the small intestine. The stomach is also enlarged, allowing for the accumulation and slow passage of food necessary for fermentation. Foregut fermentation by bacteria allows for more complete digestion of plant structural carbohydrates, but also aids in detoxification of tannins and other plant secondary compounds (Estes 1991).

Zanzibar red colobuses derive most of their water from their leaf diet, but water drinking is seen in some populations. Most notable is the discovery of frequent water drinking in populations of P. kirkii inhabiting mangrove swamps on Uzi island (Nowak 2008). Frequent water drinking emerged during confinement of these populations in mangrove refugia following displacement from their previous coral-rag forest habitat, and it is thought to be an adaptive response to the high salt intake that comes with feeding on mangrove species. Water was obtained in a number of ways, including licking rain off leaves, drinking from coral rock crevices, licking dew, and drinking from tree holes. The strategies for obtaining water were group-specific and are likely the result of learning (Nowak 2008).

Zanzibar red colobuses are the only non-human primates known to consume charcoal (Struhsaker et al. 1997). Charcoal is eaten from a variety of sources, including tree stumps, logs, and branches charred from fires associated with local swidden agriculture, as well as from kilns used by humans to burn charcoal. At least four populations in Jozani National Park and neighboring shambas consume charcoal, but not all populations eat charcoal, possibly because charcoal is not readily available in all habitats. The extent of charcoal consumption also appears to be related to diet differences among P. kirkii populations, as shamba populations have diets containing three times more phenolics than those of forest populations, primarily because of their exploitation of exotic food plants. An estimated 0.25 to 2.5 g of charcoal/kg of body weight is ingested daily (Struhsaker et al. 1997). Individuals of both sexes and all age classes have been observed to eat charcoal, and the behavior is thought to be socially transmitted by learning.

Charcoal consumption may be functionally analogous to geophagy observed in other colobines because charcoal serves as an adsorbent of potential toxins and antifeedants that may interfere with digestion (Cooney and Struhsaker 1997). Laboratory studies have shown that the charcoals eaten by P. kirkii adsorb potentially toxic materials such as phenolics and are 11 to 39% as effective as commercially manufactured activated charcoal for human consumption (Cooney and Struhsaker 1997). Charcoal consumption has allowed P. kirkii populations to exploit exotic food sources, such as Indian almond (Terminalia catappa), mango, and cassava leaves (Manihot esculenta), which, although high in toxins and antifeedants, are also of high nutritional value, being relatively high in protein and easily digestible (Struhsaker et al. 1997). Charcoal consumption is also thought to play a role in another unique feeding habit of P. kirkii, for this species is the only colobus monkey known to feed on cycads (Encephalartos hildebrandtii) (Nowak and Lee 2011b). Cycads contain carcinogenic and neurotoxic compounds such as cycasin and macrozamin, and ingested charcoal is most likely important in the immobilization of these harmful compounds (Nowak and Lee 2011b). (Cooney and Struhsaker, 1997; Estes, 1991; Nowak and Lee, 2011b; Nowak, 2008; Struhsaker, 2010; Struhsaker, et al., 1997; Walz, 2006)

• Primary Diet
• herbivore
  • folivore

• Plant Foods
• leaves
• seeds, grains, and nuts
• fruit
• flowers

Predation

Zanzibar red colobuses do not currently have any non-human predators, but the now-extinct Zanzibar leopard (Panthera pardus adersi) was historically a predator (Nowak et al. 2008). Though Zanzibar leopards were officially declared extinct in 2012, it has most likely been extinct since the 1990s (Goldman and Walsh 2002). It is possible that young animals are taken by large snakes and raptors. (Goldman and Walsh, 2002; Nowak, et al., 2008)

• Known Predators

  • Zanzibar leopards (Panthera pardus adersi) (extinct)

Ecosystem Roles

Zanzibar red colobuses are one of Zanzibar’s five primate species, along with lesser bushbabies (Galago senegalensis zanzibaricus), greater bushbabies (Otolemur garnetti garnetti), vervet monkeys (Cercopithecus aethiops nesiotes), and Sykes monkeys (Cercopithecus albogularis) (Pakenham 1984). Zanzibar red colobuses are one of the main folivores and frugivores in the coral-rag forest ecosystem, and may, like other colobines, play a role in seed dispersal (though no official study has been conducted on this subject).

While mainland Piliocolobus species are commonly observed to form interspecific associations, P. kirkii has not been found to associate extensively with other species, with one possible exception. Sykes monkeys (Cercopithecus albogularis) appear to use P. kirkii as a distracting shield against harassment and hunting by humans in agricultural areas. Sykes monkeys are harassed and sometimes killed by humans because of their crop raiding, whereas P. kirkii are not because they rarely feed on crops. It has thus been suggested that Sykes monkeys associate with Zanzibar red colobuses in shamba farmland areas because the larger and noisier red colobus groups serve as a distraction against human detection (Siex and Struhsaker 1999a; Struhsaker 2010). There have also been surprising reports of Jozani populations of P. kirkii grooming cattle in shamba farmland areas (Ho 2011), but it is unclear how common this behavior is.

Zoonotic diseases have not been studied in P. kirkii, but Uganda red colobuses (Piliocolobus tephrosceles) host a variety of diseases, including simian immunodeficiency virus (SIV), simian T-cell lymphotrophic virus (STLV), and simian foamy virus (SFV). African colobines are generally undersampled as potential hosts of primate retroviruses, and future studies may reveal greater importance of the colobines as hosts for zoonotic diseases (Goldberg et al. 2009). (Goldberg, et al., 2009; Ho, 2011; Pakenham, 1984; Siex and Struhsaker, 1999b; Struhsaker, 2010)

Economic Importance for Humans: Positive

Zanzibar red colobuses play an important role in tourism, which is one of Zanzibar's most important economic sectors (Siex and Struhsaker 1999a; Struhsaker 2005). By 2000, many thousands of tourists were visiting Jozani National Park to see these primates, generating at least $100,000 in park fees annually (Siex 2003). This income not only supports Jozani National Park, but also benefits the government and the local community. Tourists also spend much more throughout the island on transport, food, and lodging, thereby providing increased employment opportunities (Siex and Struhsaker 1999a).

Zanzibar red colobuses have also been the subject of 19 years of intermittent research beginning in the 1980s in Jozani National Park (Struhsaker 2010). Research on the populations in Kiwengwa and on the Uzi and Vundwe Islands was begun more recently in 2003 (Nowak 2008). (Nowak, 2008; Siex and Struhsaker, 1999b; Siex, 2003; Struhsaker, 2005; Struhsaker, 2010)

• Positive Impacts
• ecotourism
• research and education

Economic Importance for Humans: Negative

In the past, farmers living near Jozani National Park have complained about crop raiding by Zanzibar red colobuses, but the evidence for this behavior is controversial. In the late 1990s, farmers claimed that they were consuming coconuts in agricultural areas and requested compensation and removal of the Zanzibar red colobuses (Siex and Struhsaker 1999a). Scientific investigation of the problem found that Zanzibar red colobus consumption of coconuts was positively correlated with harvest, maybe due to a pruning effect (Siex and Struhsaker 1999a). This example illustrates the importance of scientifically quantifying perceived human-wildlife conflicts so that appropriate measures can be taken (Struhsaker 2005). There have also been reports of crop damage to mangoes and breadfruit by P. kirkii. However, it is possible that most (if not all) damage is caused by Sykes monkeys and blamed incorrectly on Zanzibar red colobuses, as the more secretive and inconspicuous Sykes monkeys often associate with groups of Zanzibar red colobuses (Siex and Struhsaker 1999a). (Siex and Struhsaker, 1999b; Struhsaker, 2005)

Conservation Status

Zanzibar red colobuses are endangered not only because of the low number of individuals, but also because of its limited and highly fragmented distribution. Various estimates of the total P. kirkii population in all its localities indicate that in 2007 its numbers were 2,000 to 2,500 individuals (Struhsaker and Siex 1998; Struhsaker 2005). The only significant populations are restricted to small, isolated pockets of forests on Unguja Island. Though they have been legally protected since 1919, less than 2% of Unguja Island is set aside for the conservation of indigenous flora and fauna (Siex and Struhsaker 1999a). The largest and only officially protected population of P. kirkii occurs in Jozani‐Chwaka Bay National Park. Approximately half of the population on Unguja reside permanently outside protected areas, many within agricultural areas. The greatest threat to populations outside protected areas is habitat loss caused by expanding agriculture and increasing demands for firewood, charcoal, and timber (Struhsaker 2005). This habitat loss has resulted in population compression of P. kirkii at Jozani with negative impacts on some of their food species (Siex 2003). Zanzibar red colobuses are occasionally killed as perceived agricultural pests. Conservation of this species is thus strongly dependent on the development of effective management plans that address the potential human-wildlife conflicts in these agricultural areas (Siex and Struhsaker 1999a).

Uzi and Vundwe Islands also contain a behaviorally and ecologically unique population of P. kirkii. The conservation status of the Zanzibar Red Colobus and its habitat on these islands is critical, as farmers were reported in 2009 to have killed at least 50 monkeys by poisoning and netting because they are perceived as crop raiders ("Update on habitat loss, conservation status of the endangered Zanzibar Red Colobus on Uzi, and Vundwe Islands" 2009). The destruction of coral-rag forest habitat is also an extensive and continuing threat. Recommendations for conservation of the Red Colobus on these islands include the gazetting of southern Uzi and Vundwe Islands as forest reserves, and the establishment of a community-based forest conservation project involving tourism (Struhsaker 2005; Nowak and Lee 2011a). ("Update on habitat loss and conservation status of the endangered Zanzibar red colobus on Uzi and Vundwe Islands", 2009; Nowak and Lee, 2011a; Siex and Struhsaker, 1999b; Siex, 2003; Struhsaker and Siex, 1998; Struhsaker and Siex, 2011; Struhsaker, 2005)

• IUCN Red List

  Endangered

• US Federal List

  No special status

• CITES

  Appendix I

• State of Michigan List

  No special status

Other Comments

Piliocolobus kirkii was named a species by Gray in 1868. It was named after Sir John Kirk, the Governor General of Zanzibar, who was the first to raise awareness about the species. Kiswahili names for Zanzibar red colobuses are "punju" and "kima mweupe," meaning “poison” and “white colobus,” respectively.

Piliocolobus monkeys are distributed across equatorial Africa from Gambia to Zanzibar in a fragmented manner (Struhsaker 2010). The classification of the 18 different ‘forms’ of Piliocolobus was one of longest standing unresolved issues in African primate taxonomy. Phylogenies were constructed using morphology, pelage, and vocalizations, but the first molecular phylogeny for the African colobines was only produced in 2008 (Ting 2008). As colobines that are morphologically similar to extant forms do not appear in the fossil record until the early Pleistocene, it was thought that extant African colobines had recent origins and diverged only after the extinction of the diverse Plio-Pleistocene colobines (Struhsaker 2010). Ting’s (2008) molecular phylogeny showed that the three modern colobine genera (Colobus, Procolobus, and Piliocolobus) diverged from one another by the late Miocene. Colobus (black-and-white colobuses) seems to have split from the other genera by 7.5 million years ago (mya) Piliocolobus (red colobuses) and Procolobus (olive colobuses) share a sister taxon relationship and also diverged from one another by the late Miocene, around 6.4 mya The three major clades in Piliocolobus seem to have separated by 3.0 mya Piliocolobus kirkii is within a clade containing Piliocolobus oustaleti (Central African red colobus), Piliocolobus rufomitratus (Tana River red colobus), and Piliocolobus tephrosceles (Ugandan red colobus), and their split occurred by 1.4 mya. Within this clade is the sister taxon relationship between P. kirkii and Piliocolobus gordonorum (Udzungwa red colobus), the split between these two sister taxa occurred 0.6 mya (Ting 2008).

Morphometric studies of P. kirkii show that the species has experienced accelerated morphological evolution of size, probably as a result of insularity. Piliocolobus kirkii is the smallest of the red colobus species, both in body size and cranium size. This observation is consistent with the island rule, which is the expectation that large mammals may become smaller on islands. There also appears to have been a concomitant decrease in body size sexual dimorphism in accordance with Rensch’s rule - the tendency for sexual dimorphism to reduce as body size decreases (Nowak et al. 2008). (Nowak, et al., 2008; Struhsaker, 2010; Ting, 2008)

Contributors

Josephine Smit (author), Yale University, Eric Sargis (editor), Yale University, Rachel Racicot (editor), Yale University, Tanya Dewey (editor), University of Michigan-Ann Arbor.

References

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