|Scientific Name:||Alouatta belzebul|
|Species Authority:||(Linnaeus, 1766)|
|Taxonomic Notes:||Hill (1962) listed five subspecies of the Red-handed Howler Monkey, Alouatta belzebul: A. b. belzebul (Linnaeus, 1766) (restricted by Cabrera  to the Rio Capim, eastern Pará); A. b. discolor (Spix, 1823) from Gurupá, Pará; A. b. ululata Elliot, 1912, from Miritiba, Maranhão; A. b. mexianae Hagmann 1908, from the island of Mexiana, in the Marajó Archipelago, Brazil; and A. b. nigerrima Lönnberg, 1941 (restricted by Cabrera  to Patinga, Amazonas).
Cruz Lima (1945) listed the form nigerrima Lönnberg 1941 as a full species. Cytogenetic studies also indicated that A. b. nigerrima is sufficiently distinct as to warrant species status (Armada et al. 1987; see also Lima and Seuánez 1989), and that it is more closely related to seniculus than to belzebul (see Oliveira 1996). Groves (2001, 2005) and Gregorin (2006) list it as a distinct species.
The taxonomy and distributions of A. belzebul have been reviewed by Langguth et al. (1987), Bonvicino et al. (1989) and Gregorin (2006). Groves (2001, 2005) did not recognize any subspecies for A. belzebul: the forms discolor, mexianae and ululata were given as junior synonyms of A. belzebul (Linnaeus, 1766). Here we follow Gregorin (2006) who recognized the forms belzebul, discolor, and ululata as full species and placed mexianae as a junior synonym of A. discolor.
|Red List Category & Criteria:||Vulnerable A2cd ver 3.1|
|Assessor(s):||Veiga, L.M., Kierulff, C. & de Oliveira, M.M.|
|Reviewer(s):||Mittermeier, R.A. & Rylands, A.B. (Primate Red List Authority)|
Listed as Vulnerable as there is reason to believe the species has declined by at least 30% over the past 36 years (three generations) due primarily to hunting and habitat loss. The isolated subpopulation in the Atlantic Forest is in a much more critical condition with only 200 individuals surviving.
Alouatta belzebul occurs in the lower Amazon, states of Amapá, Pará and Maranhão and in north-east Brazil, in the Atlantic forest of the states of Rio Grande do Norte, Piauí, Pernambucoo, Paraiba and Alagoas. It occurs in a small area of southern Amapá and on the islands of Marajó and Caviana in the Amazon estuary. It is limited to the east of the rios Xingu and Iriri. The range limits of Alouatta discolor and A. belzebul south along the lower Amazon are poorly understood and confused. Bonvicino et al. (1989) attributed the howler monkeys on Marajo and the other islands of the Amazon estuary to the form discolor, but Fernandes (1994) subsequently identified the howlers on the islands of Marajó, Caviana and Mexiana as A. belzebul (Gurupá, he found, was occupied by Alouatta macconelli). Gregorin (2006), likewise identified A. belzebul as the howler occupying Marajo, Caviana and Mexiana. Bonvicino et al. (1989) also identified a howler from the Rio Pracupy, Portel (their locality number 35) just south of the estuary as A. discolor. Ferrari and Lopes (1996) suggested, and Gregorin (2006) confirmed, its identity as A. belzebul, and not A. discolor. This would mean that discolor would be confined to a narrow strip to the immediate south of the Rio Amazonas extending west from Gurupá, across the Xingu.
Coimbra-Filho et al. (1995) argued that A. belzebul once occurred throughout the north-east (except the coastal populations now ascribed to A. ululata) as far as the left (north) bank of the Rio São Francisco. Neiva and Penna (1916) recorded the species on southern Piaui at the beginning of the early 20th century (see Coimbra-Filho et al. 1995). They have been eliminated from a large part of this range by hunting and the almost total elimination of their forests (Coimbra-Filho and Câmara 1996).
Native:Brazil (Alagoas, Maranhão, Pará, Paraíba, Pernambuco, Rio Grande do Norte, Sergipe, Tocantins)
|Range Map:||Click here to open the map viewer and explore range.|
|Population:||Extremely common in some areas (such as Marajó), but very rare in the Atlantic Forest portion of the range (Rio Grande do Norte, Alagoas, Paraíba and Pernambuco). There are around 200 individuals surving in a total of 10 isolated locations: six populations in Paraiba, two in Rio Grande de Norte, one in Pernambuco, and one in Alagoas. The largest population in the Atlantic Forest is in Pacatuba in Paraiba with about 80 animals. There have been five registered local extirpations from forest fragments in the last 50 years.|
|Habitat and Ecology:||
Occurs in a mix of habitats including lowland Amazon rainforest, Marajó várzea forest, and fragments of the northern Atlantic Forest.
The howler monkeys are the large leaf-eaters of the South American primate communities. The molar teeth are particularly adapted for their chewing leaves through shearing. Like the spider monkeys, they are prehensile-tailed, with a naked patch of skin on the under surface at the tip. Their most characteristic feature is the deep jaws which surround the enlarged larynx and hyoid apparatus, a resonating chamber. It is with this enlarged and highly specialized voice box that they produce their howls (grunts, roars and barks). Howling sessions, usually involving the entire group, can be heard particularly in the early morning and are audible at distances of 1-2 km (Drubbel and Gautier 1993).
Fourteen is a large group, and they can usually be seen numbering four or five or up to 11 or so individuals. There is usually only one dominant male in the group (occasionally two), others being sub-adults, or juveniles, along with a harem of two to five females. Unlike the spider monkeys, and related to the large proportion of leaves in the diet (up to 50% of the annual diet), the howler monkeys generally have quite small and broadly overlapping home ranges, of 5 ha up to 45 ha, depending on the type of habitat (Neville et al. 1988). Pina et al. (2002) studied two groups of 5-6 and 7-9 individuals (each with just one adult male and two adult females), with home ranges of 13.5 ha and 18.05 ha, respectively.
Howlers are the only New World primates which regularly include mature leaves in their diet, although softer, less fibrous, young leaves are preferred when they are available. Their folivory and ability to eat mature leaves is undoubtedly one of the keys to their wide distribution and the wide variety of vegetation types they inhabit. Mature fruit is the other important food item, especially wild figs (Ficus) in many regions, but they also eat leaf petioles, buds, flowers (sometimes seasonally very important), seeds, moss, stems and twigs, and termitaria. The diet of two A. belzebul groups in the Caxiuanã National Forest was studied by Souza et al. (2002). They were largely folivorous but would switch to fruits whenever available, especially during the wet season.
Adult male weight 7.27 kg (n=27), adult female weight 5.52 kg (n=26) (Peres 1994a)
Adult male weight 6.5-8.0 kg (mean 7.3 kg, n=27), adult female weight 4.85-6.2 kg (mean 5.5 kg, n=26) (Ford and Davis 1992).
|Major Threat(s):||In the Amazon, the species is widespread, although they are hunted. The Amazon populations have suffered severely from forest loss throughout their range in southern Pará over the last decade. In the Atlantic Forest population, the major threat is the fragility of the remaining small forest patches to stochastic and demographic affects (habitat loss and fragmentation has been mainly due to sugar-cane plantations).|
In the Atlantic Forest, the species occurs in Guaribas Biological Reserve, Paraiba (2,71 ha) (re-introduced), RPPN Pacatuba, and RPPN Mata da Estrela. In the Amazon, it occurs in a number of protected areas, including Caxiuanã National Forest (200,000 ha) (see Jardim and Oliveira 1997; Pina et al. 2002), Gurupí Biological Reserve (272,379 ha) and Tapirapé Biological Reserve (99,703 ha).
It is listed on Appendix II of CITES.
Armada, J. L. A., Barroso, C. M. L., Lima, M. M. C., Muniz, J. A. P. C. and Seuánez, H. N. 1987. Chromosome studies in Alouatta belzebul. American Journal of Primatology 13: 283-296.
Bonvicino, C. R. 1989. Ecologia e comprtamento de Alouatta belzebul (Primates: Cebidae) na Mata Atlântica. Revista Nordestina de Biologia 6(2): 149-179.
Bonvicino, C. R., Langguth, A. and Mittermeier, R. A. 1989. A study of the pelage color and geographic distribution in Alouatta belzebul (Primates: Cebidae). Rev. Nordestina Bio 6(2): 139-148.
Cabrera, A. 1957. Catálogo de los mamíferos de América del Sur: I (Metatheria-Unguiculata-Carnivora). Revista del Museo Argentino de Ciencias Naturales "Bernardino Rivadivia" e Instituto Nacional de Investigación de las Ciencias Naturales, Ciencias Zoológicas 4(1): 1-307.
Coimbra-Filho, A. F. and Câmara, I. de G. 1996. Os Limites Originais do Bioma Mata Atlântica na Região Nordeste do Brasil. Fundação Brasileira para a Conservação da Natureza, Rio de Janeiro, Brazil.
Coimbra-Filho, A. F., Câmara, I. de G. and Rylands, A. B. 1995. On the geographic distribution of the red-handed howling monkey, Alouatta belzebul, in North-east Brazil. Neotropical Primates 3(4): 176–179.
da Cruz Lima, E. 1945. Mammals of Amazônia, Vol. 1. General Introduction and Primates. Contribuições do Museu Paraense Emílio Goeldi de História Natural e Etnografia, Belém do Pará, Brazil.
de Jardim, M. M. A. and de Oliveira, L. F. B. 1997. Uso de espaço de Alouatta belzebul (Primates, Cebidae) em função da temporalidade de recursos. In: P. L. B. Lisboa (ed.), Caxiuanã, pp. 417-436. Museu Paraense Emílio Goeldi, Belém, Brazil.
de Jardim, M. M. A. and de Oliveira, L. F. B. 2002. Vocaliazação de um grupo de guaribas (Alouatta belzebul). In: P. L. B. Lisboa (ed.), Caxiuanã: Populações Tradicionais, Meio Físico e Diversidade Biológica, pp. 697-703. Museu Paraense Emílio Goeldi, Belém, Brazil.
Drubbel, R. V. and Gautier, J.-P. 1993. On the occurrence of nocturnal and diurnal loud calls, differing in structure and duration, in red howlers (Alouatta seniculus) of French Guyana. Folia Primatologica 60: 195–209.
Fernandes, M. E. B. 1994. Notes on the geographic distribution of howling monkeys in the Marajó Archipelago, Pará, Brazil. International Journal of Primatology 15(4): 919–926.
Ferrari, S. F. and Lopes, M. A. 1996. Primate populations in eastern Amazonia. Plenum Press, New York, USA.
Ford, S. M. and Davis, L. C. 1992. Systematics and body size: Implications for feeding adaptation in New World monkeys. American Journal of Physical Anthropology 88: 415-468.
Gregorin, R. 2006. Taxonomy and geographic variation of species of the genus Alouatta Lacépède (Primates, Atelidae) in Brazil. Revista Brasileira de Zoologia 23(1): 64–144.
Groves, C. P. 2001. Primate taxonomy. Smithsonian Institution Press, Washington, DC, USA.
Groves, C. P. 2005. Order Primates. In: D. E. Wilson and D. M. Reeder (eds), Mammal Species of the World, pp. 111-184. The Johns Hopkins University Press, Baltimore, Maryland, USA.
Hill, W. C. O. 1962. Primates Comparative Anatomy and Taxonomy V. Cebidae Part B. Edinburgh University Press, Edinburgh, Scotland.
Langguth, A., Teixeira, D. M., Mittermeier, R. A. and Bonvicino, C. 1987. The red-handed howler monkey in northeastern Brazil. Primate Conservation 8: 36-39.
Lima, M. M. C. and Seuánez, H. N. 1989. Cytogenetic characterization of Alouatta belzebul with atypical pelage coloration. Folia Primatologica 52: 97-101.
Neiva, A. and Penna, B. 1916. Viagem científico pelo norte da Bahia, sudoeste de Pernambuco, sul do Piauhi e de norte a sul de Goaiz. Mem. Inst. Oswaldo Cruz, Rio de Janeiro, Brazil.
Neville, M. K., Glander, K. E., Braza, F. and Rylands, A. B. 1988. The howling monkeys, genus Alouatta. In: R. A. Mittermeier, A. B. Rylands, A. F. Coimbra-Filho an G. A. B. da Fonseca (ed.), The Ecology and Behavior of Neotropical Primates, Vol. 2, pp. 349–453. World Wildlife Fund, Washington, DC, USA.
Oliveira, E. H. C. 1996. Estudos Citogenéticos e Evolutivos nas Espécies Brasileiras e Argentinas do Gênero Alouatta Lacépède, 1799 (Primates, Atelidae). Masters Thesis, Universidade Federal do Paraná.
Peres, C. A. 1994. Which are the largest New World monkeys? Journal of Human Evolution 26: 245-249.
Pina, A. L. C. B., Souza, L. L. de S. and Ferrari, S. F. 2002. Spacing patterns of Alouatta belzebul groups. In: P. L. B. Lisboa (ed.), Caxiuanã: Populações Tradicionais, Meio Físico e Diversidade Biológica, pp. 685-695. Museu Paraense Emílio Goeldi, Belém, Brazil.
Souza, L. L. de, Pima, A. L. C. B. and Ferrari, S. F. 2002. Diet of the red-handed howler monkey (Alouatta belzebul). In: P. L. B. Lisboa (ed.), Caxiuanã: Populações Tradicionais, Meio Físico e Diversidade Biológica, pp. 669-683. Museu Paraense Emílio Goeldi, Belém, Brazil.
|Citation:||Veiga, L.M., Kierulff, C. & de Oliveira, M.M. 2008. Alouatta belzebul. The IUCN Red List of Threatened Species. Version 2014.2. <www.iucnredlist.org>. Downloaded on 29 August 2014.|
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