Alouatta belzebul, or red-handed howler monkeys, are found in Amazonian Brazil and surrounding regions, including the states in north-east Brazil (south Amapá, Maranhão, Pará, Tocantins, and Sergipe) and states in the Atlantic forest region (Pernambuco, Rio Grande do Norte, Piauí, Alagoas, and Paraíba). Islands in the Amazon estuary (Marajó, Mexiana, and Caviana) are also home to A. belzebul. While the range of this species may extend into the lower Amazon as well, it is poorly understood and often confused with that of Alouatta discolor. The presence of Alouatta belzebul has been confirmed east of the Xingu and Iriri rivers and in the Rio Pracupy, Portal.
Biogeographic Regions: neotropical (Native )
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).
Red-handed howler monkeys are one of the least studied species of all the howler monkeys. As their common name suggests, red-handed howler monkeys have reddish hands, though some may appear more yellow. Pelage varies from black to deep reddish or yellowish. Their fur is coarse and their face and distal portion of their prehensile tail are naked and black (true of all Alouatta species). Howler monkeys in general are the largest New World monkeys. In this species, tail length ranges from 58.5 to 91.5 cm. Red-handed howler monkeys are sexually dimorphic in size; male mass ranges from 6.5 to 8.0 kg, while female mass ranges from 4.85 to 6.2 kg. In length, males range from 56.5 to 63.0 cm and females from 40.0 to 65 cm; there is, however, some disagreement in the literature over these figures with another source listing a length range from 55.9 to 91.5 cm. Red-handed howlers have 36 teeth and the dental formula is I2/2 C1/1 P3/3 M3/3.
The most distinguishing feature of Alouatta species, including A. belzebul, is their deep jaws, enlarged larynx, and calcified hyoid apparatus. This highly specialized voice box produces the characteristic howls (more like grunts, barks, and roars) used for "extragroup" and "intragroup" communication.
All Alouatta species have a zygodactylous or schizodactylous grip, meaning their first two digits are opposable to the other three.
Range mass: 4.85 to 8.0 kg.
Average mass: 5.5 F, 7.3 M kg.
Range length: 40.0 to 91.5 cm.
Other Physical Features: endothermic ; homoiothermic; bilateral symmetry
Sexual Dimorphism: male larger
Red-handed howler monkeys are found in mixed forest habitats of the Brazilian Amazon, often from the canopy to the ground; the IUCN states that their habitats range from Marajó várzea forest, to lowland Amazon rainforests, and to portions of the northern Atlantic Forest. Alouatta species typically live in undisturbed or modified dry forests to rain forests, mangrove forests, wooded savannas, and gallery forests.
Range elevation: 0 to 2,500 m.
Habitat Regions: tropical ; terrestrial
Terrestrial Biomes: forest ; rainforest
Other Habitat Features: riparian
Habitat and Ecology
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. They spend up to 70% of their day lying and sitting about quietly among the branches, fermenting leaves in their enlarged caecums. 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 kms (Drubbel and Gautier 1993).
Black howler groups number 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).
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.
Oestrus lasts 2-4 days, with intervals between oestrous periods of about 17 days. Interbirth intervals are generally about 16.6 months, although they may be shortened by the death of an infant to about 10.5 months (Crockett and Sekulic 1984).
Habitat and Ecology
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).
Red-handed howler monkeys are primarily folivorous, eating young leaves and sometimes tree bark or woody twigs, but rarely flowers or mature leaves. While they are typically dietary generalists (one study found them to feed on 67 plant species in 24 families over a 45-day period), they commonly eat plants from the family Leguminosae (pea, legume, or bean family) and Moraceae (mulberry or fig family). Red-handed howler monkeys also feed on fruit during rainy seasons, making them the most frugivorous howler monkeys.
Red-handed howler monkeys exhibit geophagy, or the ingestion of soil. This occurs when the consumption of mature leaves is unavoidable during dry seasons, and does not usually occur during fruit-eating, or wet, seasons. Soil is usually taken from arboreal termitaria, probably because it is more densely packed with nutrients such as calcium, sodium, and organic carbon than on the forest floor. It is still unknown whether this is to take up nutrients from the soil during less plentiful times, or whether the soil helps to digest the mature leaves that may contain potentially poisonous compounds like tannins.
Plant Foods: leaves; wood, bark, or stems; fruit; flowers
Other Foods: detritus
Primary Diet: herbivore (Folivore , Frugivore )
Howler monkeys are important seed dispersers in tropical ecosystems. In comparison to other neotropical primates, Alouatta species commonly disperse particularly large seeds and seeds of plants restricted to canyons. The mechanism of Alouatta seed dispersal is through group defecation, where undigested or partially undigested seeds may become buried in the soil or secondarily dispersed by dung beetles. Seed dispersal by Alouatta is known to aid in forest regeneration after fragmentation or destruction by human activity.
Ecosystem Impact: disperses seeds; creates habitat
While predation is rare in large primates, there are several known predators of howler monkeys that have been extensively studied. Aerial predators are the most common, including large raptors such as eagles and hawks. Harpy eagles (Harpia harpyja) specialize on monkey prey. Alouatta species react to aerial predators by giving a warning “howl” to other members of their group and then descending from the trees and dispersing, remaining still and silent until the predator has passed.
Tayras also prey on red-handed howler monkeys, and their interaction has been well-studied. Tayras traveling on the ground elicit no reaction, but once they reach the lianas or canopy, alarm vocalizations can be heard. Tayras usually attack young or subadult individuals during the day. Red-handed howler monkeys may react with either aggression or avoidance, and most attacks are unsuccessful.
There are records of Guajá Indians in Brazil that actively hunt and eat red-handed howler monkeys (the most of any other local primate), although they are not predicted to have a significant impact on A. belzebul populations. Additionally, some research has provided evidence of felids such as jaguars, attacking howler monkeys.
- tayras (Eira barbara)
- harpy eagles (Harpia harpyja)
- hawks and eagles (Accipitridae)
- jaguars (Panthera onca)
- other felids (Felidae)
- humans (Homo sapiens)
Life History and Behavior
Red-handed howler monkeys communicate primarily through a wide variety of vocalizations (roaring, barking and grunting), specific to the type of communication involved. “Extragroup” call functions are associated with mate attraction or defense and resource defense. Males may be assessing the strength of their opponents or displaying their own dominance and possession of females. “Intragroup” call functions are associated with group coordination and alerting one’s social group of danger. While these loud call functions are found to be widespread in most primates, these mechanisms are well-studied in the genus Alouatta. It is proposed that loud howling is much less costly (energetically) than engaging in physical interaction with potential competitors for resources or mates.
Only one genus of New World monkeys, Alouatta, has fully trichromatic vision, containing genes for red, green, and blue color vision. Red-handed howler monkeys have fully trichromatic vision and perceive the world with the full visible light spectrum. In an evolutionary sense this is advantageous for selection of the best leaves and ripest fruit. Interestingly, all New World monkeys also possess a fully functional vomeronasal organ (VNO) which is used in the perception of pheromones. The VNO was originally thought to be absent in organisms with full trichromatic vision because of its loss of necessity. It was thought that if organisms can detect all color gradients, then cues about the environment and reproductive status of conspecifics can also be detected without the use of pheromones. It currently seems that this may not be the case, and A. belzebul communicate and perceive the environment with both color vision and pheromone detection.
Communication Channels: visual ; acoustic ; chemical
Other Communication Modes: choruses ; pheromones
Perception Channels: visual ; tactile ; acoustic ; chemical
There is little information on lifespan of Alouatta belzebul in the wild due to the long-term observations required. Some suggest primate longevity of captive individuals is similar to that of wild ones. Alouatta species generally have a lifespan of 15 to 20 years.
A group of A. belzebul may be as large as 20 individuals; normal groups are 4 to 11. They are polygynous and year round breeders, though some species of Alouatta have two seasonal birth peaks (thus two breeding peaks). Red-handed howler monkeys males often howl, allowing them to asses their opponents, a cheap alternative to a physical fight or chase. Other functions of long-distance calls include mate attraction and mate defense.
Mating System: polygynous
Red-handed howler monkeys breed throughout the year and have one offspring at a time (rarely twins), with a gestation period of 187 days. Females are sexually mature at 4 years of age, with estrous cycles between 13 and 24 days, and a birth interval of 1 to 2 years. Other reproductive information specific to A. belzebul (birth weight, age at which weaning occurs, ages of sexual maturity in males and females) is not available. Alouatta palliata weigh 275 to 400 grams at birth and are weaned at 10 months. Males are sexually mature in 5 years but they do not reproduce until they have achieved a dominant role in the troop.
Breeding interval: Females give birth every 1 to 2 years.
Breeding season: Red-handed howler monkeys breed throughout the year.
Range number of offspring: 1 to 2.
Average number of offspring: 1.
Average gestation period: 187 days.
Key Reproductive Features: iteroparous ; year-round breeding ; gonochoric/gonochoristic/dioecious (sexes separate); sexual ; viviparous
There is little available information on parental investment in Alouatta belzebul. In general, howler monkey males and females leave their parent's troop after they gain independence to form new troops and achieve a better position than in a previously established hierarchy. Infanticide has been observed in other Alouatta species when a dominant male takes over a new troop. Females invest heavily in young through gestation, lactation, and care of the young.
One study suggested as members of the troop ages, the females that give birth learn from others in the troop. They suggested that differences in parturition and the handling of neonates between two groups of red-handed howlers may reflect this learning.
Parental Investment: altricial ; pre-fertilization (Provisioning, Protecting: Female); pre-hatching/birth (Provisioning: Female, Protecting: Female); pre-weaning/fledging (Provisioning: Female, Protecting: Female); pre-independence (Provisioning: Female, Protecting: Female); extended period of juvenile learning
Red-handed howler monkeys are listed as vulnerable because of a 30% population decline in the past 36 years (3 generations). This is primarily due to hunting and habitat destruction from agriculture and logging. Because they are dietary generalists and opportunistic foragers, they can adapt more easily to habitat changes and are not as affected by the habitat destruction as are other species in the genus Alouatta. Habitat fragmentation and population isolation have less of an impact on A. belzebul because of their relatively small home range sizes. In an experimental study containing logged and unlogged plots, red-handed howler monkeys did not show significant changes in activity or diet. Many local Brazilian communities have taken steps to manage logging more effectively as well as create venues of ecotourism in order to maintain howler monkey habitats and populations in the Amazon.
US Federal List: no special status
CITES: no special status
IUCN Red List of Threatened Species: least concern
IUCN Red List Assessment
Red List Category
Red List Criteria
IUCN Red List Assessment
Red List Category
Red List Criteria
It is listed on Appendix II of CITES.
Relevance to Humans and Ecosystems
Howler and spider monkeys (family Atelidae) are not generally considered agricultural pests. All non-human primates can spread pathogens to humans (and vice versa) due to close genetic relationships. The spread of viruses, bacteria, fungi, and parasites among these groups may occur though airborne or fluid transmission, physical contact (scratches or bites), handling or ingestion of tissues, and arthropod vectors.
Negative Impacts: injures humans (causes disease in humans , carries human disease)
Due to their large body size and loud calls, A. belzebul are easy to hunt or capture for commercial export. Extensive genetic and medical research projects have used A. belzebul as test subjects to study gene flow, natural selection, genetic drift, mutations within species, population genetics, experimental drugs and cures for life long illnesses like AIDS and cancer.
In 1999 at the Twenty-Second Annual Meeting of the American Society of Primatologists, Loretta Ann Cormier discussed her work on red-handed howler monkeys. She found that they are significant to the diet, religion, and social structure of indigenous peoples. Red-handed howler monkeys and 6 other species of primates found in Amazonian Brazil are primarily eaten during the wet season. The Guajá believe all monkeys are kin, and they always take in infants of mothers that were killed for food and treat them as their children. Some people feel there is a contradiction between family and food, but the religion of the Guajá people portrays this symbolic cannibalism as a religious way of life.
Positive Impacts: food ; research and education
The red-handed howler (Alouatta belzebul) is a vulnerable species of howler monkey, a type of New World monkey. It is endemic to Brazil, found in the southeastern Amazon and disjunctly in the Atlantic Forest between Rio Grande do Norte and Sergipe.
Considerable taxonomic confusion has surrounded this species. Until 2001, most authorities included the Amazon black howler as a subspecies (or simply a taxonomically insignificant variation) of the red-handed howler, though its distinction had already been pointed out much earlier. The red-handed howler remained variable in ecology, colour and pattern of the fur, shape of the cranium, and shape of the hyoid bone (of great importance in the voice of the howler monkeys; a likely isolating mechanism between the species), but a geographical pattern was not clear, resulting in it being treated as a monotypic species. In 2006, a major review of the Brazilian members of the genus Alouatta was able to match some of the variations to geography (though further study was recommended), resulting in the recognition of the Spix's red-handed howler and Maranhão red-handed howler as species separate from the red-handed howler. Even with these as separate species, the colour and pattern of the fur of the red-handed howler remains variable. Most adults are black with reddish-brown hands, feet and distal part of their tails, but some are entirely black (resembling the Amazon black howler), reddish (resembling the red howlers) or somewhere in between.
Distribution and life history
It lives in the biomes of Amazonian and Atlantic forests which consist of dense forest separated by drier areas. These animals can live up to 20 years, and do not mature until later in their lives, have a long gestation period, and generally reproduce slower than similar-sized mammals of other species. From the births that have been recorded, red-handed howlers have quick, quiet births during the day when they are normally active. Once born, if the mother is experienced, she will carry her young ventrally for three weeks and then switch to dorsally once the offspring is slightly more developed.
Behavior and diet
When not foraging, red-handed howlers rest in the canopy of mature trees 20 m (66 ft) from the forest floor. They also live in social groups of seven to 12 members, with one or two mature males, females, juveniles, and infants.
Threats to this species are numerous. First, they are a large-bodied mammal hunted for food. Females with young are especially good targets for hunting because the babies can be sold as pets and the mothers can be used for their meat. Slower reproduction of these mammals also prevents them from replenishing the population in response to this pressure. The red-handed howler monkey has one of the smallest ranges of their genus, which makes them even more susceptible to threats. Second, the Trans-Amazonia and the Belém-Brasília Highways intersect their habitats, which causes collisions with automobiles. Third, the threat from agriculture is increasing. Increasing population pressures have forced farmers to clear more land for farming and these clear-cut methods are too much of a disturbance for the red-handed howler. Some small disturbances are tolerated by species that focus more on leaves, but since A. belzebul is mostly frugivorous, it is harder for them to adapt to change. Logging is yet another concern, because it not only disrupts the habitat too much, but it also allows better access to their habitats for hunters by use of the access roads. Fourth, habitat fragmentation accompanies all of these disturbances. If the forest does eventually regenerate, there will still be no way for new howlers to come back into the area and it also prohibits gene flow and the amount of genetic variation will decrease. Lastly, predation can have a large effect on the population. Since the populations are usually in groups in small areas, they are easy prey for animals such tayras. One study found tayras had found their way onto an island and took out a large portion of the population by hunting together and preying on the family groups in the area.
A variety of options can be put into place to help the red-howler monkey recover. First, landowners can be encouraged to make sanctuaries or protect vital habitats. Since this species relies so heavily on fruit, certain habitats with a variety of fruit-producing tree stands should be focused on for protection. Second, if slash-and-burn methods are needed, farmers could use smaller portions of forest and rotate often to allow for forest regeneration and repopulation by howlers. Corridors could also be maintained between properties, crop areas, and developed areas. Success has also been documented on the use of ladder bridges across roads to allow red-handed howlers to cross roads safely. Third, translocation is could be used to repopulate suitable habitat the animals may not be able to reach because of fragmentation. Translocation could also be a useful tool in allowing gene flow between populations that would generally not mix. Lastly, the genetics of the populations should be monitored to make sure adequate genetic variability is present to sustain the populations. Some of these studies are already being done using microsatellite loci to determine diversity.
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