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Alouatta belzebulred-handed howler monkey

By Meg Wallen and Jenna Lande

Geographic Range

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. (Grzimek, 2003; Veiga, et al., 2008)

Habitat

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. ("Capuchin-like Monkey Species", 2001; "New World Encyclopedia", 2006; Veiga, et al., 2008)

  • Range elevation
    0 to 2,500 m
    0.00 to ft

Physical Description

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. (Camargo and Ferrari, 2007a; Grzimek, 1990; Grzimek, 2003)

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. (Oliveira and Ades, 2004; Veiga, et al., 2008)

All Alouatta species have a zygodactylous or schizodactylous grip, meaning their first two digits are opposable to the other three. ("New World Encyclopedia", 2006; "ZipcodeZoo.com", 2003; Grzimek, 2003; Youlatos, 1999)

  • Sexual Dimorphism
  • male larger
  • Range mass
    4.85 to 8.0 kg
    10.68 to 17.62 lb
  • Average mass
    5.5 F, 7.3 M kg
    lb
  • Range length
    40.0 to 91.5 cm
    15.75 to 36.02 in

Reproduction

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. ("Capuchin-like Monkey Species", 2001; Grzimek, 1990; Grzimek, 2003; Marsh and Mittermeier, 1987; Nowak, 1990; Oliveira and Ades, 2004; Sekulic and Chivers, 1986; Veiga, et al., 2008)

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. (Grzimek, 2003; Marsh and Mittermeier, 1987; Nowak, 1990)

  • 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

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. ("Capuchin-like Monkey Species", 2001; Grzimek, 2003; Nowak, 1990)

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. (Camargo and Ferrari, 2007b)

  • 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

Lifespan/Longevity

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. ("ZipcodeZoo.com", 2003; University of Wisconson - Madison, et al., 2009)

Behavior

Howler monkeys are diurnal, although they spend most of their day (up to 80%) sleeping in the branches with their troop members. They are arboreal and, when awake, howler monkeys move through the trees in search of food using quadrupedal locomotion. Though their tails are strong enough to support their entire body weight, they rarely use them for this, normally keeping hold with at least two appendages when moving. Red-handed howler monkeys are usually found living in small social groups ranging from 5 to 14 individuals. These groups consist of a harem with one (sometimes two) dominant male and 2 to 5 females, along with juveniles or sub-adults. (Camargo and Ferrari, 2007b; Pinto, et al., 2003; Veiga, et al., 2008; Whitehead, 1995)

Probably the best-known behavioral characteristic of red-handed howler monkeys (and howler monkeys in general) is their extremely loud vocalization calls, or howling sessions. An enlarged hyoid bone and modified voice box allows for the loud, deep calls to be heard from up to 2 km away. These howling sessions usually occur in the mornings and involve the entire social group. Whitehead (1995) classifies most Alouatta species, including A. belzebul, loud calls as “non-palliata,” with a wide range of frequencies (300 to 2000 Hz) and a more sustained call duration, as opposed to the lower frequency range and shorter call duration of Alouatta palliata. (Pinto, et al., 2003; Veiga, et al., 2008; Whitehead, 1995)

  • Range territory size
    50000 to 450000 m^2
  • Average territory size
    170000 m^2

Home Range

The known home range of howler monkeys is 13 to 18 ha, although it is estimated to vary between 5 and 45 ha, depending on the location and habitat type. Home ranges overlap among members of the same social groups, yet there is also some observed overlap between different social groups. Home ranges of A. belzebul are not known to be severely affected by logging or destruction of forests. (Pinto, et al., 2003; Veiga, et al., 2008)

Communication and Perception

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. (Grzimek, 2003; Nowak, 1990; Oliveira and Ades, 2004; Sekulic and Chivers, 1986)

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. (Webb, et al., 2004)

Food Habits

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. (De Souza, et al., 2002; Ferrari, et al., 2008; Pinto and Setz, 2004; Pinto, et al., 2003)

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. (De Souza, et al., 2002; Ferrari, et al., 2008; Pinto and Setz, 2004; Pinto, et al., 2003)

  • Plant Foods
  • leaves
  • wood, bark, or stems
  • fruit
  • flowers

Predation

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. (Camargo and Ferrari, 2007a; Cormier, 2003; Miranda, et al., 2006)

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. (Camargo and Ferrari, 2007a; Cormier, 2003; Miranda, et al., 2006)

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. (Camargo and Ferrari, 2007a; Cormier, 2003; Miranda, et al., 2006)

Ecosystem Roles

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. (Moura and McConkey, 2007; Ponce-Santizo, et al., 2006)

  • Ecosystem Impact
  • disperses seeds
  • creates habitat

Economic Importance for Humans: Positive

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. (Grzimek, 2003; Nowak, 1990)

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. (Cormier, 1999)

  • Positive Impacts
  • food
  • research and education

Economic Importance for Humans: Negative

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. ("New World Encyclopedia", 2006; "New World Encyclopedia", 2006; "Non-Human Primates", 2008)

Conservation Status

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. (Horwich, 1998; Pinto, et al., 2003; Veiga, et al., 2008)

Other Comments

Alouatta species were previously classified in the family Cebidae. The geological age of this taxon is approximately 40 million years old. (Marsh and Mittermeier, 1987; Nowak, 1990)

Contributors

Meg Wallen (author), University of Michigan-Ann Arbor, Jenna Lande (author), University of Michigan-Ann Arbor, Phil Myers (editor, instructor), Museum of Zoology, University of Michigan-Ann Arbor, Tanya Dewey (editor), Animal Diversity Web.

Glossary

Neotropical

living in the southern part of the New World. In other words, Central and South America.

World Map

acoustic

uses sound to communicate

altricial

young are born in a relatively underdeveloped state; they are unable to feed or care for themselves or locomote independently for a period of time after birth/hatching. In birds, naked and helpless after hatching.

arboreal

Referring to an animal that lives in trees; tree-climbing.

bilateral symmetry

having body symmetry such that the animal can be divided in one plane into two mirror-image halves. Animals with bilateral symmetry have dorsal and ventral sides, as well as anterior and posterior ends. Synapomorphy of the Bilateria.

causes disease in humans

an animal which directly causes disease in humans. For example, diseases caused by infection of filarial nematodes (elephantiasis and river blindness).

chemical

uses smells or other chemicals to communicate

choruses

to jointly display, usually with sounds, at the same time as two or more other individuals of the same or different species

crepuscular

active at dawn and dusk

detritus

particles of organic material from dead and decomposing organisms. Detritus is the result of the activity of decomposers (organisms that decompose organic material).

diurnal
  1. active during the day, 2. lasting for one day.
endothermic

animals that use metabolically generated heat to regulate body temperature independently of ambient temperature. Endothermy is a synapomorphy of the Mammalia, although it may have arisen in a (now extinct) synapsid ancestor; the fossil record does not distinguish these possibilities. Convergent in birds.

folivore

an animal that mainly eats leaves.

food

A substance that provides both nutrients and energy to a living thing.

forest

forest biomes are dominated by trees, otherwise forest biomes can vary widely in amount of precipitation and seasonality.

frugivore

an animal that mainly eats fruit

herbivore

An animal that eats mainly plants or parts of plants.

iteroparous

offspring are produced in more than one group (litters, clutches, etc.) and across multiple seasons (or other periods hospitable to reproduction). Iteroparous animals must, by definition, survive over multiple seasons (or periodic condition changes).

motile

having the capacity to move from one place to another.

native range

the area in which the animal is naturally found, the region in which it is endemic.

pheromones

chemicals released into air or water that are detected by and responded to by other animals of the same species

polygynous

having more than one female as a mate at one time

rainforest

rainforests, both temperate and tropical, are dominated by trees often forming a closed canopy with little light reaching the ground. Epiphytes and climbing plants are also abundant. Precipitation is typically not limiting, but may be somewhat seasonal.

riparian

Referring to something living or located adjacent to a waterbody (usually, but not always, a river or stream).

sedentary

remains in the same area

sexual

reproduction that includes combining the genetic contribution of two individuals, a male and a female

social

associates with others of its species; forms social groups.

swamp

a wetland area that may be permanently or intermittently covered in water, often dominated by woody vegetation.

tactile

uses touch to communicate

terrestrial

Living on the ground.

tropical

the region of the earth that surrounds the equator, from 23.5 degrees north to 23.5 degrees south.

visual

uses sight to communicate

viviparous

reproduction in which fertilization and development take place within the female body and the developing embryo derives nourishment from the female.

year-round breeding

breeding takes place throughout the year

References

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BayScience Foundation, Inc. 2003. "ZipcodeZoo.com" (On-line). Alouatta (Genus). Accessed March 31, 2009 at http://zipcodezoo.com/Key/Animalia/Alouatta_Genus.asp.

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Camargo, C., S. Ferrari. 2007. Interactions between tayras (Eira barbara) and red-handed howlers (Alouatta belzebul) in eastern Amazonia. Primates, 48: 147-150.

Cormier, L. 2003. Kinship with Monkeys: The Guaja Foragers of Eastern Amazonia. New York: Columbia University Press.

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Ferrari, S., L. Veiga, B. Urbani. 2008. Geophagy in new world monkeys (Platyrrhini): ecological and geographic patterns. Folia Primatol, 79: 402-415.

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Grzimek, B. 1990. Simians (Cebids: Comparison of Species). Pp. 174 in S Parker, ed. Grzimek's Encyclopedia of Mammals, Vol. 2nd, 1st Edition. New York: McGraw-Hill Publishing Company.

Gursky, S., K. Nekaris. 2007. Primate Anti-Predator Strategies. New York, NY: Springer.

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Marsh, C., R. Mittermeier. 1987. Primate Conservation in the Tropical Rain Forest: Monographs in Primatology, Volume 9. New York: Alan R. Liss, Inc..

Miranda, J., I. Bernardi, R. Moro-Rios, F. Passos. 2006. Antipredator behavior of brown howlers attacked by black hawk-eagle in southern Brazil. International Journal of Primatology, 27: 1097-1101.

Moura, A., K. McConkey. 2007. The capuchin, the howler, and the Caatinga: seed dispersal by monkeys in a threatened Brazilian forest. American Journal of Primatology, 69: 220-226.

Nowak, R. 1990. Walker's Primates of the World. Baltimore and London: The John Hopkins University Press.

Oliveira, D., C. Ades. 2004. Long-distance calls in Neotropical primates. Anais da Academia Brasileira de Ciencias, 76: 393-398.

Pinto, A., C. Azevedo-Ramos, O. de Carvalho Jr.. 2003. Activity patterns and diet of the howler monkey Alouatta belzebul in areas of logged and unlogged forest in eastern Amazonia. Animal Biodiversity and Conservation, 26: 39-49.

Pinto, L., E. Setz. 2004. Diet of Alouatta belzebul discolor in an Amazonian rain forest of northern Mato Grosso State, Brazil. International Journal of Primatology, 25: 1197-1211.

Ponce-Santizo, G., E. Andresen, E. Cano. 2006. Dispersiόn primaria de semillas por primates y dispersiόn secundaria por escarabajos coprόfagos en Tikal, Guatemala. Biotropica, 38: 390-397.

Sekulic, R., D. Chivers. 1986. The significance of call duration in howler monkeys. International Journal of Primatology, 7: 183-190.

University of Wisconson - Madison, , Wisconson Primate Research Center Library, National Primate Research Center. 2009. "Primate Info Net" (On-line). The Life Spans of Nonhuman Primates. Accessed March 31, 2009 at http://pin.primate.wisc.edu/aboutp/phys/lifespan.html.

Veiga, L., C. Kierulff, M. de Oliveira. 2008. "2008 IUCN Red List of Threatened Species" (On-line). Alouatta belzebul. Accessed March 21, 2009 at www.iucnredlist.org.

Webb, D., L. Cortes-Ortiz, J. Zhang. 2004. Genetic evidence for the coexistence of pheromone perception and full trichromatic vision in howler monkeys. Molecular Biology and Evolution, 21: 697-704.

Whitehead, J. 1995. Vox Alouattinae: A preliminary survey of the acoustic characteristics of long-distance calls of howling monkeys. International Journal of Primatology, 16: 121-144.

Youlatos, D. 1999. The schizodactylous grasp of the howling monkey. Zeitschrift fuer Morphologie und Anthropologie, Vol. 82/Issue 2-3: 187-198.

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