Lophocebus albigena (Gray, 1850)

Russell A. Mittermeier, Anthony B. Rylands & Don E. Wilson, 2013, Cercopithecidae, Handbook of the Mammals of the World – Volume 3 Primates, Barcelona: Lynx Edicions, pp. 550-755 : 655-656

32.

Gray-cheeked Mangabey

Lophocebus albigena

French: Lophocébe a joues grises / German: Grauwangenmangabe / Spanish: Mangabey de mejillas grises

Other common names: Cloaked Mangabey, White-cheeked Mangabey

Taxonomy. Presbytis albigena Gray, 1850 ,

Democratic Republic of Congo, Mayombe.

The genus Lophocebus was separated from Cercocebus and subsequently split into L. albigena and L. aterrimus . In 2007, C. P. Groves elevated three subspecies of L. albigena to full species, based on morphological characters and color of the shoulder mantle: gray in L. albigena , reddish-brown in L. osmani , and brown to straw-colored in L. johnstoni . Groves also recognized a fourth species ( L. ugandae ) based on skull morphology and smaller size. Some experts consider the grayer, coastal Cameroon population to be a distinct subspecies (L. a. zenkeri), although differences would seem to be more likely clinal in nature. Distributions of L. albigena and L. osmani might overlap in south-eastern Cameroon, and L. albigena possibly hybridizes with L. osmani in the Dja Biosphere Reserve, Cameroon, but is probably geographically separated from L. johnstoni by the Ubangi River and from L. aterrimus by the Congo River. Albinism is known in this species. Monotypic.

Distribution. S Cameroon (S of Sanaga River), SW Central African Republic (W of Ubangi River), Equatorial Guinea, Gabon, Republic of the Congo (E to Ubangi River).

Descriptive notes. Head-body 45-73 cm (males) and 50-56 cm (females), tail 73— 100 cm (males) and 67-80 cm (females); weight 6.1-9 kg (males) and 4.7-6.5 kg (females). As in other species of crested mangabeys ( Lophocebus ), fur of the Gray-cheeked Mangabey is soft and long, being generally blackish-brown. A long, pale mantle on shoulders (more prominent in males) runs continuous with rather thin, grayish cheek whiskers. There is a short, partially upright tuft on the crown, and eyebrows tend to stand upright in two little “horns.” Tail is long and ragged, and it is normally carried straight up with the tip arched forward over the back. Face is black. Female Graycheeked Mangabeys have more slender builds than males and develop a conspicuous pink swelling when sexually receptive.

Habitat. Low-elevation primary and secondary rainforest, gallery forest, and some swamp forest. The Gray-cheeked Mangabey is mosttypically found in dense evergreen forest, where it prefers the middle and upperlayers of the forest canopy.

Food and Feeding. As in otherspecies of crested mangabeys, the diets of Gray-cheeked Mangabeys consist mainly offruits (30-60%) and seeds (29-36%). Theyalso eat young leaves, bark, flowers, and animal prey (invertebrates and small vertebrates). Animal prey makes up 27% of the diet at Dja, Cameroon, 13% at Mondika, Central African Republic, and 25% at Lopé in Gabon.

Breeding. Female Gray-cheeked Mangabeys exhibit a bright pink genital swelling when sexually receptive. Ovarian cycleslast c.31 days. A single young is born every 2-4 yearsafter a gestation of 184-189 days. At birth, the naked parts of the face, ears, and ischial callosities are flesh-colored. Infants are weaned at 7-10 months. Females are sexually mature at three years of age and males at 5-7 years. Interbirth intervals average ¢.30 months, but they are shorterif the infant dies. Individuals may live for more than 20 years in captivity.

Activity patterns. Gray-cheeked Mangabeys are diurnal and arboreal. Depending on the time of year, groups forage for 42-54% of the day, travel for 20-28%, rest for 10-28%, and engage in social activities for 6-8%.

Movements, Home range and Social organization. Gray-cheeked Mangabeys live in multimale-multifemale groups of ¢.20 individuals (range 6-30). In larger groups, there may be as many as 6-11 males. Studies at Mondika in the Central African Republic recorded daily movements of ¢.1137 m. A group used 167 ha over the course of a year. Home ranges are variable in size but are generally large, 100-400 ha, and overlap extensively with other groups. Groups show a tendency to avoid each other. Large groups may split, and smaller subgroups can travel and forage separately for as long as three weeks at a time. In captivity, males and females form dominance hierarchies. Males usually leave their natal groups at maturity. As in other species of crested mangabeys, Gray-cheeked Mangabeys give a species-typical, low-pitched loud call (“whoop-gobble”), produced using an extralaryngeal resonating air sac. This loud call can be heard 500-1200 m away. They whoop, pause for aboutfive seconds, and then gobble for about three seconds. When they whoop, their body jerks forward slightly, lips remain closed and are pushed forward into a pout, and cheeks billow out. Theysit tense and attentive, the shoulders shake slightly, and the eyes are half closed. When gobbling, their shoulders shake up and down, their mouth is closed, and their head is slightly raised. These loud calls are given especially by high-ranking individuals. Gray-cheeked Mangabeys grunt a lot and in numerous contexts; e.g. when feeding, resting, traveling, approaching other individuals, or after copulation. Grunts vary in intensity from soft and slow to loud and rapid. Chuckles (or repeated staccato barks) are given in a variety of alarm or surprise situations such as the appearance of duikers (Cephalophus), suids such as Forest Hogs (Hylochoerus meinertzhageni) and Red River Hogs (Potamochoerus porcus), raptors, and other possible predators. Predators include the crowned hawk-eagle (Stephanoaetus coronatus) and Chimpanzees (Pan troglodytes). Population densities range from 10 ind/km? to 20 ind/km? in Cameroon and Gabon. Like other species of crested mangabey, the Gray-cheeked Mangabeyis often found in polyspecific associations with arboreal guenons ( Cercopithecus ), red colobus ( Piliocolobus ), and black-and-white Colobus (Colobus) . In a number ofareas, it is sympatric with the Red-capped Mangabey ( Cercocebus torquatus ) or the Agile Mangabey (C. agilis ).

Status and Conservation. CITES Appendix II. Classified as Least Concern on The [UCN Red List. The IUCN Red List recognizes the form zenkeri (not considered here) as a subspecies of the Gray-cheeked Mangabey. The Gray-cheeked Mangabeyis listed as Class B in the African Convention on the Conservation of Nature and Natural Resources. It is hunted for food in some areas and occasionally shot as a crop pest. Destruction and conversion of forest habitats also constitute threats. Gray-cheeked Mangabeys are known to occur in various protected areas: Dja Biosphere Reserve, Douala-Edéa Wildlife Reserve, and Campo-Ma’an, Boumba-Bek, Nki, and Lobéké national parks in Cameroon; Rio Campo, Monte Alen, and Los Altos de Nsork national parks in Equatorial Guinea; Loango, Lopé, and Minkebé national parks in Gabon; Nouabalé-Ndoki and Odzala national parks in the Republic of Congo; and Dzanga-Ndoki National Park and Ngotto Classified Forest Reserve in the Central African Republic.

Bibliography. Bermejo (1999), Blois-Heulin (1999), Blois-Heulin & Martinez-Cruz (2005), Blom et al. (1992), Brown (2011), Brugiére et al. (2002), Carroll (1986), Cashner (1972), Chapman et al. (1999), Colyn (1994), Cronin & Sarich (1976), Deputte (1986, 1991), Fleagle (1999), Fleagle & McGraw (2002), Frost et al. (2003), Gautier-Hion (1975), Gautier-Hion & Brugiére (2005), Gautier-Hion & Gautier (1976, 1986), Gautier-Hion et al. (1999), Gilbert (2008), Groves (1978, 2001, 2005b, 2006b, 2007a), Grubb (2006), Ham (1994), Harris (2000), Harris & Disotell (1998), Hill (1974), Horn (1987a), Jolly (2007), Jones & Sabater Pi (1968), Kingdon (1997), Matthews & Matthews (2002), McGraw et al. (2012), Mitani (1990, 1991), Oates (2011), Poulsen & Clark (2001), Poulsen, Clark, Connor & Smith (2002), Poulsen, Clark & Smith (2001), Quris (1976), Shah (2003), Stuart & Stuart (2006), Swedell (2011), Tutin & White (1998), Tutin et al. (1997), Usongo & Fimbel (1995).

Figures

On following pages: 16. Arunachal Macaque (Macaca munzala); 17. Tibetan Macaque (Macaca thibetana); 18. Stump-tailed Macaque Macaca arctoides); 19. Long-tailed Macaque (Macaca fascicularis); 20. Rhesus Macaque (Macaca mulatta); 21. Japanese Macaque (Macaca fuscata); 22. Taiwanese Macaque (Macaca cyclopis).

Distribution. S Cameroon (S of Sanaga River), SW Central African Republic (W of Ubangi River), Equatorial Guinea, Gabon, Republic of the Congo (E to Ubangi River).