Lagothrix lagothricha (Humboldt, 1812)

Russell A. Mittermeier, Anthony B. Rylands & Don E. Wilson, 2013, Atelidae, Handbook of the Mammals of the World – Volume 3 Primates, Barcelona: Lynx Edicions, pp. 484-549 : 545

20 .

Humboldt’s Woolly Monkey

Lagothrix lagothricha

French: Lagotriche de Humboldt / German: Brauner Wollaffe / Spanish: Mono lanudo pardo Other common names: Common Woolly Monkey; Brown Woolly Monkey (lagothricha), Colombian Woolly Monkey (lugens)

Taxonomy. Simia lagothricha Humboldt, 1812 ,

Colombia, Rio Guaviare, above the mouth of the Rio Amanaveni, Guainia .

Although the genus was revised by C. P. Groves in 2001 to include four species ( L. lagothricha , L. lugens , L. poeppiggii, and L. cana ) rather than the one species with four subspecies as earlier defined by]J. Fooden in 1963, Colombian studies of phenotype, karyotypes, and the mitochondrial COII gene strongly suggest that at least lagothricha and lugens belong to the same species and should be considered subspecies of L. lagothricha . The subspecies lagothricha appears to intergrade with lugens west of the Rio Caguan in the Caqueta Department, Colombia. Two subspecies recognized.

Subspecies and Distribution. L. lL. lagothricha Humboldt, 1812 — SE Colombia, NE Ecuador, NW Brazil, and N Peru, from the Cordillera Oriental, N of the rios Napo and Amazonas, to the Rio Uva, a N bank affluent of the Rio Guaviare (Vichada Department, Colombia), E to the Rio Orinoco and upper Rio Negro to the Venezuelan border and NW Brazil; it is not known if it occurs in Venezuela. L. [. lugens Elliot, 1907 — Colombia, E of the Rio Atrato, throughout the Cordillera Oriental, W of the Rio Ariari (Meta Department), and parts of the Cordillera Central to the northernmost parts of the Serrania de San Lucas (SE Bolivar & N Antioquia departments), in some places up to elevations of 3000 m, and northward in the piedmont forest (now mostly destroyed) to the Rio Arauca (Arauca Department); there is no evidence thatits occurs in neighboring SW Venezuela.

Descriptive notes. Head-body 46-65 cm (males) and 46-58 cm (females), tail 53— 77 cm (males) and 62-72 cm (females); weight of males ¢.7 kg (but when dominant they become more robust and can weigh as much as 10 kg) and of females 5-7 kg. Humboldt’s Woolly Monkey is quite variable in color, from very light blond (locally known as “churucos blancos” or white woollies) in the Amazon Basin to a very uniform dark brown (almost black) in the Cordillera Central. Generally, individuals are some shade of brown above, sometimes with a slightly paler head, dark gray hands and feet, and often ajet-black underside of long chest hair in adults. The area between shoulder blades can be paler than shoulders, and there is occasionally some ticking on lower legs, arms, and tail. There may be a coronalstripe of lighter tone or even blond on the head in both subspecies. In the Amazon, some individuals have blond tufts around the base of the tail. Males are larger than females, with longer canines, and well-developed masseter muscles on either side of the head. The clitoris is as long as or longer than the penis, and adult testicles are very prominent. The original description of the two subspecies is generally inadequate to distinguish them because of variability of tones and overlap of characteristics purported to belong to each. Pelage morphs of the “Brown Woolly Monkey” (L. l. lagothricha ) in the lowlands are actually a mosaic (not a cline) of different morphs that vary from very light blond to very dark brown with many individuals in between the two extremes. Generally, the “Colombian Woolly Monkey” (L. I. lugens ) tends to have darker tones of brown than are typical of the Brown Woolly Monkey, culminating in the holotypic charcoal animals of the Cordillera Central of the Andes. Many individuals of both subspecies have ticked or agouti forearms and forelegs, long black chest hair (in adults), and coronalstripes.

Habitat. Primary, secondary, flooded, and non-flooded lowland rainforest and primary and secondary montane forest up to elevations of 3000 m. Humboldt’s Woolly Monkeys use the middle and upper forest canopy. They can be found in wide (several kilometers) Colombian piedmont gallery forests, but most of these populations have been extirpated in what are now destroyed and fragmented forests.

Food and Feeding. Humboldt’'s Woolly Monkeys feed mainly on ripe, fleshy, endozoochorous fruits, supplemented with young leaves, flowers, gums, seeds, palm nuts, and invertebrate prey. They exploit well over 200 species of fruits during the year; 185 species were tabulated in a study in eastern Colombia, while more than 220 species were identified in diets in forests west of the Rio Duda, western Colombian Amazon. In the study in eastern Colombia where soils are very poor, the diet consists of 78-9% fleshy fruits, 11:4% leaves, 4-9% invertebrates, 4-3% seeds, 0-3% bark, 0-1% flowers, and 0-1% tendrils. The most important species were Chrysophyllum amazonicum ( Sapotaceae ) at 10-3% of the fruit-feeding records, Manilkara amazonica ( Sapotaceae ) at 5%, Iriartea ventricosa ( Arecaceae ) at 2:2%, Cheiloclinium sp. (Celastraceae) at 22%, and Protium sp. (Burseraceae) at 2%. The most important families were Sapotaceae , Moraceae , and Fabaceae , followed by 38 other families. At the Rio Duda site, the most interesting differences were that Moraceae was the most important family rather than Sapotaceae (ninth in importance) and the consumption of invertebrates (12%) was much higher at Rio Duda. These differences might be explained by highersoilfertility, because species of Moraceae seems to increase in importance on better soils and the availability of invertebrates might increase where better soils support increased primary production. Another explanation for higher invertebrate consumption could be differences in data collection techniques. Humboldt’s Woolly Monkeys tend to spend the most time feeding on sweet and succulent fruits from abundant plants that produce large fruit crops. During fruit scarcity, they prefer large trees that fruit during times of scarcity and that have fruits with a high pulp-to-seed ratio, low lipid content, and clumped distributions. Results from one study suggest that Humboldt’s Woolly Monkeys are generalized, opportunistic frugivores that avoid some fruits with secondary compounds.

Breeding. Female Humboldt’s Woolly Monkeys are sexually mature at c.6 years of age. They generally leave their natal group for another group at this time, although some evidence suggests that dominant females remain in their natal group. Mating begins soon after a female enters a new group. Males sometimes approach and follow receptive females, but females frequently follow males and solicit mating. Mating occurs throughout the year, resulting in births year-round, but with a peak when food is plentiful during the early rainy season (March—May) in the eastern Colombian Amazon and late rainy season to early dry season (July-December) in the western Colombian Amazon. All sexually mature males have access to the group’s females and copulate with them, but the number of copulations is positively correlated with the linear hierarchy among males. During copulation, both sexes give a special vocalization (click or “tooth chatter”), a rhythmical movement of the teeth with maximal exposure. Copulation is dorsal ventral, with the male behind the female and the female reclining on the branch. Copulation lasts 6-7 minutes. All adult males may mate with a receptive female, but the dominant male copulates most. Dependent young climb over the copulating individuals and look at the pair’s genitalia. Females emigrate from their group to a neighboring group at c.6 years of age and usually begin copulating soon after. There are very low levels of aggression toward new females, perhaps because they are quickly accepted by adult males. A single offspring is born after a gestation of 223-225 days. In a twelve-year study, females were found to have a 23-36-day reproductive cycle, with a birth interval averaging 36-7 months. Following birth, the female has a period of sexual inactivity averaging 23-4 months, but sexual activity, when reassumed, continues for an average of 7-2 months before she conceives again. Copulation can occur at any time, but there are times when females copulate more frequently; this is in December—May in the western Colombian Amazon. During copulation periods, cycles last 2:3-3-1 days (when copulation is frequent) interspersed by 11-3-14-7-day intervals with no mating. After conception, copulations become non-cyclic. Births are usually singleton, occasionally twins. Neonates are nursed for up to a year. They are carried ventrally at first but move to the mothers’ back after c.2 weeks. Adult males sometimes participate, carrying an infant on their back and actively guarding it. Both sexes are fully mature at c.8 years, but the first parturition is usually at c.9 years. Humboldt’s Woolly Monkeys may live for more than 30 years; the population under study at the Rio Duda site in Colombia includes a 31-year-old individual.

Activity patterns. Humboldt’s Woolly Monkeys are diurnal and arboreal, spending most of their time in the middle and upper forest canopy. Activity budgets calculated in two studies were resting 29-9% and 23-2%, moving 38-8% and 34-5%, foraging 25-8% and 36-2%), and other activities 5-5 and 6-1% (the first values from a population in a very infertile, poor forest and the second from a population in a rich, fertile forest closer to the Andes). The woolly monkeys evidently were able to travel and forage less and rest more in rich forest.

Movements, Home range and Social organization. Humboldt’s Woolly Monkeys live in patrilineal social groups; only females move between groups, while males are philopatric. Depending on the availability of ripe fruit, a group moves 1000-3500 m/day and occupies home ranges of 169-800 ha. Average daily movement for a group of 24 individuals in eastern Colombia was 2880 m in a home range of 760 ha. A group of 17 individuals in the Rio Dudasite, western Colombian Amazon, traveled 1633 m/day and occupied a smaller home range of 169 ha. Differences in home range size and daily movement of the two groups were probably due to differences in the quality of the two forests where they were found.

Status and Conservation. CITES Appendix II. Classified as Vulnerable on The IUCN Red List, only as the Humboldt’s Woolly Monkey. The Colombian Woolly Monkey is classified as a distinct species ( L. lugens ) and Critically Endangered on The IUCN Red List. Humboldt’s Woolly Monkeys are intensively hunted, especially by indigenous people, because their meatis considered delicious and their fat is used in cooking and for supposed medicinal purposes. They are also frequently kept as pets, with the mother typically being shot to obtain the infant. Humboldt’s Woolly Monkeys are known to occur in Pico da Neblina National Park and Juami-Japura Ecological Reserve in Brazil; Amacayacu, Cahuinari, La Paya, and Serrania de Chiribiquete national natural parks and Nukak National Natural Reserve in Colombia; and Sumaco-Napo Galeras National Park, Cayambe-Coca and Cofan-Bermejo ecological reserves, and Cuyabeno Wildlife Reserve in Ecuador. Nevertheless, at least in Brazil and Colombia, indigenous peoples have the right to hunt them even in protected areas. In Colombia, presence of any indigenous settlement eventually results in extirpation of Humboldt’s Woolly Monkeys in a radius of several kilometers.

Bibliography. Botero et al. (2010), Defler (1989a, 1995, 1996, 1999a, 2003a, 2003b, 2010), Defler & Defler (1996), Fooden (1963), Groves (2001), Milton & Nessimian (1984), Nishimura (1988, 1990, 2003), Nishimura et al. (1992), Nunez-Iturri & Howe (2007), Palacios et al. (2008), Parathian & Maldonado (2010), Peres & Palacios (2007), Ruiz-Garcia (2005), Ruiz-Garcia & Pinedo-Castro (2010), Stevenson (1992, 1997a, 1997b, 1998, 2000, 2001, 2002, 2003, 2004, 2006), Stevenson & Ahumada (1994), Stevenson & Aldana (2008), Stevenson & Castellanos (2000), Stevenson & Guzmaéan-Caro (2010), Stevenson & del Pilar-Medina (2003), Stevenson & Quinones (1993), Stevenson,Castellanos et al. (2002), Stevenson, Pineda & Samper (2005), Stevenson, Quinones & Ahumada (1994, 1998, 2000).

Figures

On following pages 21 Gray Woo ly Monkey (Lagothnx cana) 22 Poeopıg s Woolly Monkey (Layothnx poøpplgll) 23 Pefuvıan Yellow taıled Woolly Monkey (Oreonıx Ilavıaıuda) 24 Southern Munquı (Brachyreles ııachnoıdes) 25 Nonhem Munqu (Brachyteles hypoxanthusl

Subspecies and Distribution. L. lL. lagothricha Humboldt, 1812 — SE Colombia , NE Ecuador , NW Brazil , and N Peru , from the Cordillera Oriental, N of the rios Napo and Amazonas, to the Rio Uva, a N bank affluent of the Rio Guaviare (Vichada Department, Colombia ), E to the Rio Orinoco and upper Rio Negro to the Venezuelan border and NW Brazil ; it is not known if it occurs in Venezuela . L. [. lugens Elliot, 1907 — Colombia , E of the Rio Atrato, throughout the Cordillera Oriental, W of the Rio Ariari (Meta Department), and parts of the Cordillera Central to the northernmost parts of the Serrania de San Lucas (SE Bolivar & N Antioquia departments), in some places up to elevations of 3000 m, and northward in the piedmont forest (now mostly destroyed) to the Rio Arauca (Arauca Department); there is no evidence thatits occurs in neighboring SW Venezuela .