Alouatta seniculus (Linnaeus, 1766)

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 : 525

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Colombian Red Howler

Alouatta seniculus

French: Hurleur roux / German: Roter Brillaffe / Spanish: Mono aullador rojo Other common names: Red Howler, Red Howling Monkey, Venezuelan Red Howler; Jurua Red Howler (juara), Purus Red Howler (puruensis)

Taxonomy. Simia seniculus Linnaeus, 1766 ,

Cartagena, department of Bolivar, Colombia .

In 1962, W. C. O. Hill listed nine subspecies of A. seniculus : seniculus , arctoidea , stramineus, macconnell, insulanus, amazonica, Juara, puruensis, and sara . The type specimen of A. s. stramineus is a female Paraguayan Howler ( Alouatta caraya ) and hence not a valid name for a red howler. Populations considered to be the domain of stramineus were attributed to A. macconnelli by C. P. Groves in 2001; he concluded that macconnelli and sara were valid species but that arctoidea and juara were subspecies of A. seniculus , amazonica and puruensis were synonyms of juara, and insulanus (from Trinidad Island) was a synonym of A. macconnelli . In his study of the morphology of the Brazilian howlers (cranium, hyoid, and pelage color patterns), R. Gregorin argued that juara and puruensis should be classified as distinct species. Distributions of these two forms are poorly understood, and here (contrary to Groves regarding puruensis) they are recognized as subspecies of A. seniculus pending further studies. A genetic study by R. Stanyon and coworkers in 1995 concluded that arctoidea was a full species, and it is considered so here. Three subspecies recognized.

Subspecies and Distribution. A. s. seniculus Linnaeus, 1766 — Colombia wherever there is forest (except along the Pacific coast and in the desert of the Guajira Peninsula in the far N), NW Venezuela (around Lake Maracaibo), Amazonian Brazil (N of the Solimoes and S of the Rio Negro), E Ecuador and E Peru (E of the Andes, E of the Rio Huallaga,to the upper rios Maranon, Napo, and Putumayo). A. s. juara Elliot, 1910 = W Amazonian Brazil S of the Solimoes, extending W into Amazonian Peru, in the Jurua Basin and, considering the form amazonica to be a synonym, extending across the Rio Solimoes to the interfluvium of the rios Japura and Negro; the W limit defining its distribution is not known. A. s. puruensis Lonnberg, 1941 — Brazilian Amazon, from the Rio Jurua Basin E to the lower Rio Madeira and the middle Rio Aripuana, it extends E across the upper Aripuana to the Rio Teles Pires, to the S is restricted to the N of the Rio Abuna, a left bank tributary of the Rio Madeira that extends along the N border of Bolivia; its occurrence is uncertain in the N of Rondonia State, S of the Rio Ji-parana, although it occurs in S Rondonia, to the Rio Mamoré-Guaporé, in the Serra da Pacaas Novos, and E through the Serra dos Parecis to the Rio Teles Pires.

Descriptive notes. Head-body 51-63 cm (males) and 48-57 cm (females), tail 57- 80 cm (males) and 52-69 cm (females); weight 5-4-9 kg (males) and 4-1-7 kg (females). The nominate subspecies of the Colombian Red Howler ( seniculus ) is strongly sexually dimorphic. Overall,it is golden-toned to coppery-red on the body, contrasting with a maroon head, shoulders, limbs, and proximal part of the tail. Crown hairs run completely forward, meeting backward-directed forehead hairs in a forwardly concave “V.” In general, males are much bigger than females and often have a blackish beard, limbs, and tail. Coat color ranges from old gold to deep golden-red, with the head (including the beard), shoulders, limbs, and proximal part of the tail deep maroon—the latter becoming paler along its length and with the tip nearly as light as the body. The face is black. Some individuals from Venezuela are almost entirely purplish-red. The “Jurua Red Howler” (A. s. juara) is not sexually dichromatic. It is a dark reddish-brown, with a small area in the middle of the back a little lighter in color (orangey-rufous). Limbs and base of the tail are dark rufous to black. Thetail is paler, more golden, from the middle to the tip. The “Purus Red Howler” (A. s. puruensis) is sexually dichromatic. Males are dark rufous (red brown) with a golden color on the upper dorsum (around the shoulder blades), whereas females are golden-orange, with distal portions of their limbs, base of theirtails, and their beards dark rufous.

Habitat. All types of forested environments including mangroves along the Caribbean coast, humid, semi-deciduous, and deciduous forest, and cloud forest (including oak forest in Colombia). Colombian Red Howlers occur in gallery and riparian forests in the Eastern Llanos of Colombia. They are found from sea level to cloud forest at elevations up to 3200 m in the Central Andes, Colombia. Although occurring in all forest types in the Amazon, Colombian Red Howlers are sometimes very rare or absent in terra firma forests. They prefer productive alluvial plains and flooded forest, particularly those flooded annually by silt-rich white water (varzea). Their preferences for flooded forests and mineral licks were given as the reason for their comparative rarity at numeroussites surveyed in Rondonia. Colombian Red Howlers were absent or very scarce in terra firma forests where species of Lagothrix and Ateles were still abundant in the interface between Amazon forest and savanna vegetation in southern Rondonia.

Food and Feeding. Colombian Red Howlers in Venezuela and Colombia eat fruit (70% of ingested plant material by dry weight), with young leaves, flowers, and mature leaves making up the rest. A study by H. L. Queiroz in the varzea of Lago Mamiraua, Mamiraua Sustainable Development Reserve in Brazil, estimated a diet of 47-3% fruits (ingested with insects), 25-6% mature leaves, 19-9% young leaves, and 7-2% miscellaneous items, including flowers. Fig trees, especially Ficus trigona ( Moraceae ), often dominate the diet, supplying young and mature leaves and fruits. Weevil larvae in fig fruits (average 2-3 larvae/fruit) also provide protein. Besides Ficus , the four most important plants in annual diets of Colombian Red Howlers at Lago Mamiraua were Coussapoa (Urticaceae) providing young and mature leaves and fig-like fruit, Piranhea trifoliata (Euphorbiacae) providing leaves, Neoxythece elegans (Sapotacae) providing fruit, and Pithecellobium corymbosum ( Fabaceae ) providing young leaves. At Tinigua National Natural Park, Colombia, most of the fruit in the diets of Colombian Red Howlers came from species of Brosimum , Ficus , Pseudolmedia , and Castilla (all Moraceae ). In cloud forest in Huila in the Colombian Andes, the annual diet of a group of Colombian Red Howlers was 44-5% young leaves, 42-4% fruits, 7-5% mature leaves, 5-4% flowers, and 0-2% leaf petioles. Ficus (nine species), Cecropia (Urticaceae) , Morus (Moraceae) , and Quercus (Fagaceae) were the principal genera in the diet.

Breeding. Female Colombian Red Howlers reach sexual maturity at 43-54 months, and they give birth to their first infant at ¢.60 months after a gestation of 186-194 days. Births are usually single and are not seasonal. At Pacaya-Samiria National Reserve in Peru, births occur throughout the year, with the majority in the wet season (October-April) and only a few in the dry season (May-September). Receptive periods for breeding last 2—4 days, with intervals of c.17 days. Interbirth intervals are 16-28 months, although they may be shortened by the death of an infant to ¢.10-5 months. Only females carry infants; they cling to the mothers’ ventrum until they are about one month old and are then carried on the back. By four months, they venture off their mothers to explore, and by six months old, they are carried only at moments of alarm.

Activity patterns. Colombian Red Howlers spend 67-78% of their day resting, 10- 12:7% feeding, and 4-4-5-6% traveling. At Lago Mamiraua, they spend 76-3% oftheir day resting, 16% traveling, 6% feeding, and 1-7% engaging in social or other activities. A similar pattern was noted for a group in cloud forest (elevation 2300 m): 78-5% resting, 12-7% feeding, 5-:6% traveling, and 3-2% engaging in social and other activities. Colombian Red Howlers generally occupy the middle and upper forest canopy, but occasionally they go to the ground to feed on soil or cross between forest patches. They swim across rivers and sleep in large emergenttrees.

Movements, Home range and Social organization. Groups of Colombian Red Howlers are multimale—multifemale or unimale—multifemale, with 6-13 individuals. A population studied over many years by P. Soini in Pacaya-Samiria National Reserve had mixed-sex groups, all-male groups, and solitary individuals. Mixed-sex groups had 2-11 individuals (exceptionally 13) and averaged 5-5 individuals, with 1-2 adult males and 1-3 adult females. Their home ranges were 6-9 ha. Sizes of nine groups in semi-deciduous mesic forest patches and gallery forest in the Eastern Llanos of Colombia were 3-9 individuals, with 1-3 adult males and home ranges of 10-26 ha. At Caparu on the Rio Apaporis in Colombia, a group of seven individuals, with one adult male and two adult females, used a very large home range of 182 ha, with daily movements of 370-2200 m (average 1150 m/day). Both sexes leave their natal groups. Violent fights can accompany the entry of a new dominant male into a group. A harpy eagle (Harpia harpyja) took an adult 7-3-kg male in Manu National Park and Biosphere Reserve in Peru. Queiroz and J. M. Ayres estimated densities of Jurua Red Howlers in varzea around Lago Mamiraua at the mouth of the Rio Japura at 38-39-5 ind/km?. A density of 36 ind/km? was recorded in riparian and flooded forest in Pacaya-Samiria National Reserve. C. Peres compared primate communities in terra firma forest and varzea along the Rio Jurua, Brazil. At five varzea sites, densities of Jurua Red Howlers were 24-7, 35-7, 89-7, 15-6, and 35-7 ind/km?. In terra firma forest, howlers were sometimes not seen during censuses even though they occurred there. Otherwise, densities at nine locations were 1-9-2 ind/km?. Densities of 1-1 ind/km? and 4 ind/km? were estimated at two non-hunted sites of nutrient-poor terra firma forest on the lower rios Caqueta and Apaporis in Colombia; howlers did not occur at a third site.

Status and Conservation. CITES Appendix II. Classified as Least Concern on The IUCN Red List, including all three subspecies. The Colombian Red Howler is widespread and locally common, but itis intensively hunted for meat in some areas. It occurs in numerous and many large protected areas, including Mamiraua and Amana state sustainable development reserves and Jau, Pico da Neblina, and Serra do Divisor national parks in Brazil; Amacayacu, Tinigua, Chiribiquete, El Tuparro, Paramillo, and Sierra de la Macarena national natural parks and Nukak and Puinawai national natural reserves in Colombia; and Pacaya-Samiria National Reserve and Manu National Park and Biosphere Reserve in Peru.

Bibliography. Ayres (1986a), Bodini & Pérez-Hernandez (1987), Bonvicino et al. (2001), Defler (1981, 2004), Defler et al. (2003), Gaulin & Gaulin (1982), Gregorin (2006), Gregorin et al. (2008), Groves (2001), Hernandez-Camacho & Cooper (1976), Hill (1962), Iwanaga & Ferrari (2002b), Lopez et al. (2005), Neville et al. (1988), Palacios & Peres (2005), Palacios & Rodriguez (2001), Pinto & Setz (2000), Queiroz (1995), Rylands & Brandon-Jones (1998), Sampaio etal. (1996), Seuanez et al. (2005), Sherman (1991), Soini (1992), Stanyon et al. (1995).

Figures

On following pages 2 Urs ne Red Howler (Alouatta arcroldoal 3 Guıanan Red Howler (Alouarra macconnellı) 4 Bolıvıan Red Howler (Alouatta sara) 5 Amazon Black Howler Alouatta nigerrima) 6 Red-handed Howler (Alouarta belzebul) 7 Spıx s Howler (Alouatta discolorl 8 Maranhão Red-handed Howler (Alouatta ululata)

Subspecies and Distribution. A. s. seniculus Linnaeus, 1766 — Colombia wherever there is forest (except along the Pacific coast and in the desert of the Guajira Peninsula in the far N), NW Venezuela (around Lake Maracaibo), Amazonian Brazil (N of the Solimoes and S of the Rio Negro), E Ecuador and E Peru (E of the Andes, E of the Rio Huallaga,to the upper rios Maranon, Napo, and Putumayo). A. s. juara Elliot, 1910 = W Amazonian Brazil S of the Solimoes, extending W into Amazonian Peru , in the Jurua Basin and, considering the form amazonica to be a synonym, extending across the Rio Solimoes to the interfluvium of the rios Japura and Negro; the W limit defining its distribution is not known. A. s. puruensis Lonnberg, 1941 — Brazilian Amazon, from the Rio Jurua Basin E to the lower Rio Madeira and the middle Rio Aripuana, it extends E across the upper Aripuana to the Rio Teles Pires, to the S is restricted to the N of the Rio Abuna, a left bank tributary of the Rio Madeira that extends along the N border of Bolivia ; its occurrence is uncertain in the N of Rondonia State, S of the Rio Ji-parana, although it occurs in S Rondonia, to the Rio Mamoré-Guaporé, in the Serra da Pacaas Novos, and E through the Serra dos Parecis to the Rio Teles Pires.