Alouatta belzebul
Creators: name: Russell A. Mittermeier
name: Anthony B. Rylands
name: Don E. Wilson
Publisher: name: Lynx Edicions
Year: 2013
Subjects: Biodiversity
Taxonomy
Animalia
Chordata
Mammalia
Primates
Atelidae
Alouatta
Alouatta belzebul

description: 6.
Red-handed Howler
Alouatta belzebul
French: Hurleur a mains rousses / German: Rothand-Briillaffe / Spanish: Mono aullador de manos rojas Other common names: Red-handed Howling Monkey
Taxonomy. Simia belzebul Linnaeus, 1766,
Brazil. Restricted by O. Thomas in 1911 to Pernambuco, Brazil, and subsequently restricted by A. Cabrera in 1957 to the Rio Capim, eastern Para.
In 1962, W. C. O. Hill listed five subspecies of A. belzebul (belzebul, discolor, ululata, mexianae, and nigerrima), but C. P. Groves considered all but mnigerrima as junior synonyms. Following R. Gregorin in 2006, belzebul, discolor, nigerrima, and ululata are recognized here as distinct species. The identity of mexianae is uncertain; Gregorin believed it to be a synonym of A. discolor, whereas M. Fernandes in his 1994 review of howlers of the Marajo Archipelago concluded it was a synonym of A. belzebul. Although considered an essentially Amazonian species, there are relict populations in the Atlantic Forest of north-eastern Brazil, and molecular and cytogenetic genetic analyses have shown that A. belzebul formsa sister group with A. guariba; the two are believed to have split from a common ancestor c.4 million years ago. Monotypic.
Distribution. Lower Amazonian Brazil S of the Rio Amazonas in the states of Para (also on Mexiana, Caviana, and Marajo Is in the Amazon estuary), Maranhao, Tocantins, and Mato Grosso, crossing the rios Tocantins and Araguaia W as far as the Rio Xingu-Iriri, and isolated populations in NE Brazil in the coastal regions of the states of Rio Grande do Norte, Paraiba, Pernambuco, and Alagoas (it is probable that its distribution was once continuous through the states of Ceara and Piaui to the Amazonian population). Its southern distributional limits in Para coincide with the change from tall forest to open formations such as the cerrado (bush savanna), caatinga (xeric scrub), and the babassu palm (Orbygnia) forest.
Descriptive notes. Head-body 58-65 cm (males) and 37-50 cm (females), tail 56— 70 cm (males) and 45-57 cm (females); weight 6-5-8 kg (males) and 4-8-6-2 kg (females). The Red-handed Howler has a short-haired toupee on the brows that meets a forward-directed stream (from a whorl between the nape and withers) in a low transverse crest on front of the crown. This forward stream diverges to the sides to run laterally. It is primarily black, but hands, feet, tip of the tail, and sometimes forehead and back are reddish-brown to yellow. In some areas, all individuals of one or both sexes may be uniformly black or red. The scrotum is rusty-red.
Habitat. Primary, seasonal semi-deciduous terra firma, wet evergreen and flooded forest, and some disturbed forest. The Red-handed Howler prefers the upper levels of the forest canopy.
Food and Feeding. A north-eastern population of Red-handed Howlers, studied in the Fazenda Pacatuba, Paraiba, by C. Bonvicino, was relatively frugivorous, eating fruits of 34 species, seeds of five species, flowers of five species, leaves ofsix species, and gum exuded from seed pods of Parkia pendula (Fabaceae). As is typical for howlers, fruits of the Moraceae family, especially Ficus and Brosimum, figured prominently in the diet, as did Myrtaceae (Eugenia, Campomanesia) and Fabacae (Inga). In the wet season when fruits are abundant, Red-handed Howlers spent 915% if their of time eating fruit, 2% young leaves, 2% mature leaves, and 4-5% other items, and in the dry season, 43-9% fruit, 40-8% flowers, 11% young leaves, and 4-3% mature leaves. Diets of Red-handed Howlers also were also studied in tall (canopy 40 m), terra firma forest in the Amazonian part its range, in the Caxiuana National Forest, just east of the lower Rio Xingu in Para. The diet of one group studied by M. Jardim from September (middle of the dry season) to March (middle of the wet season) indicated a diet c.70% fruit, 18% young leaves, 11% mature leaves, and 1% flowers. A subsequent study of the annual diets of two groups showed a predominance of leaves (58:5% of the diet overall), undoubtedly because it covered the late wet season and early dry season when fruit is relatively scarce. Diets were 40-5% new leaves, 36-5% fruit, 13-6% leaves of unknown age, 4-9% flowers, and 4-5% mature leaves. Leaf consumption increased when fruits were scarcer (May-August). For one of the groups, c¢.50% of the fruit feeding records came from just three species: Ficus guianensis (Moraceae) 23-2%, Ocotea cf. cernua (Lauraceae) 11:6%, and Virola sebifera (Myristicaceae) 9-8%. Red-handed Howlers also eat seeds of Vouacapoua americana (Fabaceae) and soil from termitaria during the dry season.
Breeding. Two births of Red-handed Howlers were recorded in the study in Paraiba: one in early November (early dry season) and the other in late August (late wet season). Two births were also recorded in an Amazonian population. Births occurred in the early afternoon. One of the females was seen to eat the placenta. One infant was carried ventrally for the first month and then on the mother’s back. The other infant was carried dorsally from the moment it was born. These two infants died in their second and fourth months, one possibly because of a botfly infestation.
Activity patterns. During the dry season in Paraiba, Red-handed Howlers rested for 57-7% of the day,traveled for 19-9%, fed for 119%, called for 3-4%, and groomed and played for 5-6% (other activities for 1-5%). During the wet season, they rested more (60-65%), traveled (18-4%) and fed less (8-2%), vocalized more (9:3%), and engaged in social activities less (3:6%). In the dry season, the amount of time feeding was quite consistent through the day, but in the wet season, there were morning (09:00-11:00 h) and afternoon (13:00-15:00 h) peaks. In the dry season, Red-handed Howlers were active from ¢.06:00 h to ¢.18:00 h, but in the wet season, they tended to begin their day earlier (c.05:00 h) and retire earlier (c.15:00 h). Bouts of howling were bimodal, with a strong peak in the early morning (04:00-07:00 h) and a lesser peak in the late afternoon (16:00-17:00 h). Red-handed Howlers travel and feed in the middle and upper forest canopy and sleep on the broad branches of tall emergenttrees.
Movements, Home range and Social organization. Red-handed Howlers live in unimale—multifemale or multimale-multifemale groups. In north-eastern Brazil, four groups had 5-14 individuals; all groups had a single male, exceptfor the largest group of 10-14 individuals that had two males. All groups had 2-3 adult females. Home ranges of two groups, both with 6-8 individuals, were 4-7 ha and 9-5 ha. In Caxiuana National Forest, three groups of Red-handed Howlers had single males and 5-9 individuals; home ranges were 13-5-18 ha. They used a larger portion of their home ranges in the wet season than in the dry season, associated with a more diverse diet in terms of numbers of species and trees they visited for food. The number oftrees visited in the wet season was nearly twice that in the dry season. Daily movements are similar in the two seasons, with a mean of 1328 m (range 997-2296 m) in the dry season and 1621 m (range 861-2409 m) in the wet season. Tayras (Eira barbara) were observed accompanying a group of Red-handed Howlers over a few days, eventually attacking an infant. The adult male gave alarm calls continuously but made no attempt to defend the infant. The infant was wounded, but because the Tayras moved off when they saw the human observer, it was saved. Tayras were also seen attacking a subadult female while on the ground. A number of deaths recorded at the time of these attacks were likely caused by Tayras. On an island in the man-made lake of Tucurui in Para, sightings and deaths of Red-handed Howlers suggested that a Tayra family swam across a channel to reach the island.
Status and Conservation. CITES Appendix II. Classified as Vulnerable on The IUCN Red List. The Red-handed Howler is widespread and can be locally common in the eastern Amazonian states of Para and Maranhao. It is very rare in north-eastern Brazil, where the total population is estimated at ¢.300 individuals in eleven isolated locations: seven in Paraiba, two in Rio Grande de Norte, one in Pernambuco, and one in Alagoas. The largest population of ¢.80 individuals occurs in a small area of Atlantic Forest in Pacatuba, Paraiba, surrounded by sugar cane plantations. Red-handed Howlers were reintroduced in Guaribas Biological Reserve (4322 ha), Paraiba, with translocated individuals from Sapé and Santa Rita in Paraiba and the release of local pets; the population numbered twelve individuals in 2007. The eastern Amazon in southern Para and the north of Mato Grosso has suffered devastating deforestation over the last 20 years; the timber industry, mining, infrastructure development, and agroindustry have taken a heavy toll on the forests and their associated wildlife. The Red-handed Howler is the largest primate in the region and heavily hunted. It is protected in Caxinana National Forest, what remains of the damaged Gurupi Biological Reserve, and Tapirapé Biological Reserve to the south—all in Para.
Bibliography. Armada et al. (1987), Bonvicino (1989), Bonvicino et al. (1989), Cabrera (1957), Camargo & Ferrari (2007a, 2007b), Coimbra-Filho & Camara (1996), Coimbra-Filho et al. (1995), Consigliere et al. (1998), Cortés-Ortiz et al. (2003), da Cruz Lima (1945), Fernandes (1994), Ferrari et al. (2008), Gregorin (2006), Gregorin et al. (2008), Groves (2001, 2005b), Hill (1962), Jardim & Oliveira (1997), Langguth et al. (1987), Lima & Seuanez (1989), Nascimento, Bonvicino, de Oliveira et al. (2008), Nascimento, Bonvicino, da Silva et al. (2005), Pina et al. (2002), Piso & Marcgrave (1648), Rylands et al. (1996), Sampaio et al. (1996), Schneider, Sampaio et al. (1996), Schneider, Schneider et al. (1993), de Souza, Ferrari et al. (2002), de Souza, Pina & Ferrari (2002), Thomas (1911).
description: Published as part of Russell A. Mittermeier, Anthony B. Rylands & Don E. Wilson, 2013, Atelidae, pp. 484-549 in Handbook of the Mammals of the World – Volume 3 Primates, Barcelona :Lynx Edicions on pages 527-528, DOI: 10.5281/zenodo.5727205