Overview

Brief Summary

Biology

The biology and behaviour of these primates has fascinated scientists over the years. Charles Darwin suggested that, within the vertebrates, the loudest male would attract the most females by advertising his strength (2). However, there seems little evidence of this in howler monkeys and it is now thought that their calls announce a troop's right to food trees in the forest. Unlike other howlers, this species does not give a dawn chorus and seems to reserve most of its howling for inter-group encounters (5). These loud calls therefore play a role in avoiding conflict between groups and thus in saving energy which can be better used for foraging and digestion (2) Brown howling monkeys feed mainly on leaves, flowers and fruit, though the composition of their diet varies according to the season and their location in the forest (6). During autumn and winter, individuals must also spend more time feeding due to the inferior quality of the food and the higher demands on energy in these colder months (6). Generally howlers spend over half of their waking hours resting to conserve energy for feeding. Though leaves, flowers and fruit are abundant in tropical forests, they are low in nutrients and high in cellulose and so do not provide much energy (2). Mammals lack the enzymes to digest cellulose, and while primates of the subfamily Colobinae have evolved specialised stomachs containing bacteria to digest the leaves, howlers have a simple, acid stomach similar to that of humans. However, howlers also have two enlarged sections where fermentative bacteria exist that are able to break down the material efficiently (2). In the process of fermentation, energy-rich gases (known as volatile fatty acids) are produced. Howlers absorb and use these gases as an energy source for their daily activities (2). Home ranges are small, up to around 31 hectares for a group of 15-20 individuals, as brown howling monkeys limit the distances they travel to feed (2). Males defend the home ranges by intimidation and fighting, which protects the group and allows females to invest more energy in reproduction and care of the young (2). Females usually have a single offspring, which are weaned before they are one year old (6).
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Description

Brown howling monkeys, like other howler monkeys, are best known for their impressive howls, which can be heard for over 1.6 km and are often mistaken for roars of lions by visitors to the area (2). Far from being dangerous predators, these primates are placid, arboreal vegetarians that live in social groups (2). There are ten species of howler monkeys, which can be identified by their coat colour (2) (3). As expected, brown howling monkeys have brown coats, though the colour may vary from brown to dark red or black. The hair is lighter and sparser on the belly, and the face and ears are dark and bare (2). Like other howlers, they have large stocky frames. The males are considerably larger than the females. Their tails are long and prehensile, and lack fur on the underside near the tip. These amazing features allow brown howling monkeys to hang from their tails and use them as an anchor while feeding (2) (3).
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Distribution

Range Description

This species inhabits a large part of the Atlantic forest of Brazil, south from southern Bahia (formerly south from the Rio Paraguaçú), extending south into basin of the Rio Jacuí, municipality of São Lourenço do Sul, state of Rio Grande do Sul (Printes et al. 2001), and the extreme north of Argentina in the Department of Misiones (Crespo 1954; Rylands et al. 1988; Di Bitetti et al. 1994; Rylands 1994; Marques 2003). Aguiar et al. (2007) recorded sympatry and probable hybridization with A. caraya in riparian forest along the left margin of the Rio Paraná (between Porto Figueira and Port Camargo) in the Ilhas e Várzeas do Rio Paraná Environmental Preotection Area on the state of Paraná. This region is considered to be an ecotone between Cerrado (the typical domain of A. caraya) and the Atlantic forest (A. guariba).

Kinsey (1981) argued that the Rio Doce separated a northern subspecies (the nominate) from the southern subspecies (A. g. clamitans). However, through a large part north of the Rio Doce, howler monkeys were indistinguishable from those south (S. Mendes pers. comm.). Surveys by Rylands et al. (1988) resulted in the discovery of groups just south of the lower Jequitinhonha, which were all pale gold in colour, whereas further west, north of the middle Jequitinhonha, groups in dedicuous forests showed sexual dichromatism typical of clamitans further south (females dark brown, males golden brown). North of the Jequitinhonha, there are very few records of any Brown Howler Monkeys at all, and few significant populations remain. If the uniformly pale howlers of the lower Jequitinhonha are, in fact, a distinct subspecies (the nominate), then the populations can only be miniscule. But, the validity of the two subspecies remains doubtful, and confused even with a recent genetic analysis comparing populations in the south of its range in the states of Santa Catarina, Sao Paolo and Rio de Janeiro suggesting strong subpopulation differentiation in clamitans.
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Geographic Range

Brown howlers are found on the Atlantic coast of South America, mainly in Brazil's coastal forests. They are endemic to the Atlantic Forest ecoregion of Brazil and Argentina. In Brazil, brown howlers are the only primate species on the protected island Ilha do Cardososo. In Argentina, the brown howler is found only in the Upper Parana Atlantic Forest of Misiones province.

Biogeographic Regions: neotropical (Native )

  • Chiarello, A. 1993. Activity Pattern of the Brown Howler Monkey Alouatta fusca, Geoffroy 1812, in a Forest Fragment of Southeastern Brazil. Primates, 34(3): 289-293.
  • Holzmann, I., I. Agostini, J. Areta, H. Ferreyra, P. Beldomenico, M. Di Bitetti. 2010. Impact of Yellow Fever Outbreaks on Two Howler Monkey Species (Alouatta guariba clamitans and A. caraya) in Misiones, Argentina. American Journal of Primatology, 72: 475–480.
  • Ingberman, B., R. Fusco-Costa, E. Monteiro-Filho. 2009. Population Survey and Demographic Features of a Coastal Island Population of Alouatta clamitans in Atlantic Forest, Southeastern Brazil. International Journal of Primatology, 30: 1-14.
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Range

Found in south-eastern Brazil and north-eastern Argentina in South America, and possibly in parts of Uruguay and Bolivia as well (3).
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Physical Description

Morphology

Physical Description

Brown howlers are one of the largest leaf-eating primates in the South American forests. They exhibit adaptations for folivory including molars with prominent shearing crests; however, unlike other leaf-eating primates (e.g., colobines) brown howlers do not have have elongated guts needed for processing cellulose. Like spider monkeys, they have prehensile-tails, with a naked patch of skin on the ventral surface of the tip of the tail. They have relatively large, stocky frames with pelage that varies in color from brown to dark red or black. The hair is lighter colored and less coarse on the belly, and the face and ears are dark and hairless. Brown howlers are sexually dimorphic, with males weighing 2.5 kg more than females on average. Many males have a dark-red venter, with yellowish red dorsal pelage and darker arms, legs, and tails. Adult females are covered in dark brown or reddish brown hair. A latitudinal color gradient occurs in the subspecies Alouatta guariba clamitans. Males tend to be more red in the south and less red in the north, whereas females range from lighter brown in the south to darker brown in the north.

Members of Alouatta are best known for their howls that closely resemble grunts or barks. The sound is produced in their deep jaws, which surround an enlarged larynx and hyoid apparatus. The hyoid apparatus is a resonating chamber and, in combination with a highly specialized voicebox, produces howls that can be heard 1 to 2 km away.

Range mass: 4 to 7 kg.

Average mass: Male: 6.7 Female: 4.3 kg.

Range length: 56 to 92 cm.

Other Physical Features: endothermic ; homoiothermic; bilateral symmetry

Sexual Dimorphism: male larger; sexes colored or patterned differently

  • Fleagle, J. 1988. Primate Adaptation and Evolution. New York: Academic Press.
  • Fortes, V., J. Bicca-Marques. 2007. Abnormal Pelage Color in an Isolated Population of Alouatta guariba clamitans Cabrera, 1940 in South Brazil. International Journal of Primatology, 29(3): 717–722.
  • Streier, K. 2004. Howler monkeys and spider monkeys. Pp. 155-170 in B Grzimek, S Craig, D Thoney, N Schalger, M Hutchins, eds. Grzimek's Animal Life Encyclopedia, Vol. 12, Mammals III Edition. Detroit, MI: Thomson/Gale.
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Ecology

Habitat

Habitat and Ecology

Habitat and Ecology
An inhabitant of lowland, submontane and montane forest of the Atlantic coast of Brazil, extending inland to mesophytic semideciduous seasonal forest inland in the states of São Paulo, Minas Gerais and Paraná (Rylands et al. 1988; Mendes 1985, 1989; Chiarello 1993, 1995, 1999; Marques 2001). In Paraná and Rio Grande do Sul, it occurs in the highly seasonal subtropical and temperate, mixed broadleaf/Araucaria forest (Schneider and Marques 1999; Buss 2001). Aguiar et al. (2007) recorded it in periodically flooded, seasonal, semideciduous forest in the floodplains of the Rio Paraná, Paraná.

The howler monkeys are the large leaf-eaters of the South American primate communities. The molar teeth are particularly adapted for 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 kms (Drubbel and Gautier 1993).

Brown Howler Monkeys an be seen in groups of four or five, but up to 11 or so, individuals. There is usually only one dominant male in the group (occasionally two), others being subordinate younger male, sub-adults, or juveniles, 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.

Size:
Adult male weight mean 6.73 kg (n=4) (Smith and Jungers 1997)
Adult female weight mean 4.35 kg (n=5) (Smith and Jungers 1997).

Systems
  • Terrestrial
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Brown howlers inhabit lowland, submontane and montane forests as well as inland semideciduous seasonal forests. In south-eastern Brazil, brown howlers inhabit highly seasonal subtropical and temperate forests. Brown howlers on the protected island Ilha do Cardoso State Park inhabit the subtropical and tropical Atlantic Forest, where they are often found in trees of the genus Araucaria and tend to avoid the restinga (i.e., coastal lowland savannah).

Habitat Regions: temperate ; tropical ; terrestrial

Terrestrial Biomes: forest ; rainforest

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Inhabits primary and secondary Atlantic coastal forest and often associated with 'monkey puzzle' trees (Araucaria) – an endemic species of pine (2) (3).
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Trophic Strategy

Food Habits

Brown howlers rely mostly on leaves, flowers, and fruit; however, their diet varies according to the season and location. Leaves make up close to a third of their diet and when available they prefer young leaves. The flowers and leaves of various types of lianas (i.e., any type of woody vine) are commonly ingested by brown howlers in south-eastern Brazil and make up approximately 27% of their diet. Fruit consumption depends on location and can be a significant part the brown howler diet depending on availability. When available, they preferentially select fleshy fruits. Brown howlers spend more time foraging during fall and winter, as the quality of available food decreases and more energy is required to maintain homeostasis when temperatures are low.

Plant Foods: leaves; fruit; flowers

Primary Diet: herbivore (Folivore , Frugivore )

  • Chiarello, A. 1994. Diet of the Brown Howler Monkey Alouatta fusca in a semi-deciduous Forest Fragemnt of Southeastern Brazil. Primates, 35(1): 25-34.
  • Martins, M. 2008. Fruit diet of Alouatta guariba and Brachyteles arachnoides in Southeastern Brazil: comparison of fruit type, color, and seed size. Primates, 49(1): 1-8.
  • Martins, M. 2009. Lianas as a food resource for brown howlers (Alouatta guariba) and southern muriquis (Brachyteles arachnoides) in a forest fragment. Animal Biodiversity and Conservation, 32(1): 51-58.
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Associations

Ecosystem Roles

Members of Alouatta tend to be colonial and can adapt to a wide range of modified habitats. They are frugivores and folivores and may play a significant role in dispersing the seeds or pits of a variety of plant species, including Celtis spinosa and Cordia sellowiana. Brown howlers are host to a variety of parasitic protozoa (Giardia), bacteria, and viral species that can also infect humans and livestock. Many species of roundworms including thread worms, pin worms and whip worms spend at least part of their complex life cycle in the tissues of brown howlers, as do many species of flatworms, including liver flukes and lung flukes. Increased human contact has been shown to increase the prevalence of parasites in brown howlers. Brown howlers are also known to host a number of ectoparasitic arthropods including mites, ticks, and lice

Ecosystem Impact: disperses seeds

Mutualist Species:

Commensal/Parasitic Species:

  • Kowalewski, M., T. Gillespie. 2009. Ecological and Anthropogenic Influences on Patterns of Parasitism in Free-Ranging Primates: A Meta-analysis of the Genus Alouatta. Pp. 433-461 in P Garber, A Estrada, J Bicca-Marques, E Heymann, K Strier, eds. South American Primates: Comparative Perspectives in the Study of Behavior, Ecology, and Conservation, Vol. -, IV Edition. New York: Springer.
  • Martins, M. 2006. Comparative Seed Dispersal Effectiveness of Sympatric Alouatta guariba and Brachyteles arachnoides in Southeastern Brazil. Biotropica, 38(1): 57-63.
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Predation

Neotropical primates are most frequently prey upon by birds and felids. In some areas, ocelots reportedly consume high numbers of brown howlers. Other known predators of brown howlers include feral dogs and black-hawk eagles. Brown howlers employ a variety of behavioral tactics in order to evade potential predators. For example, they often make loud vocalizations that alert group members of approaching predators. When threatened, brown howlers may hide in the forest canopy, and if the threat persists, they may escape in a line formation led by an adult. In addition, dominant males may distract approaching predators, which gives group members a chance to flee. Immobility and silence are also used as antipredatory tactics.

Known Predators:

  • Bianchi, R., S. Mendes. 2007. Ocelot (Leopardus pardalis) Predation on Primates in Caratinga Biological Station, Southeast Brazil. American Journal of Primatology, 69(10): 1173-1178.
  • 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(4): 1097-1101.
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Life History and Behavior

Behavior

Communication and Perception

Brown howler monkeys use high-amplitude calls to minimize predation, control access to resources, and for mating. They also produce loud calls to signal group strength, and by listening to the calls of rival groups, they can assess the strength of their opponents. Although most members of Alouatta perform a "dawn chorus" in the morning, brown howlers do not. The majority of calling by brown howlers occurs during intergroup encounters. Using calls to assess the strength of rival groups helps reduce direct physical confrontation.

Rubbing behavior in brown howlers serves a variety of functions. Anogenital rubbing in females, which spreads odiferous signals through feces, urine, or vaginal secretions, is hypothesized to signal reproductive status. Hyoid and sternum rubbing in males is linked to agonistic and territorial cues that signal dominance.

Communication Channels: visual ; tactile ; acoustic ; chemical

Other Communication Modes: choruses ; pheromones ; scent marks

Perception Channels: visual ; acoustic

  • Chiarello, A. 1995. Role of Loud Calls in Brown Howlers, Alouatta fusca. American Journal of Primatology, 36(3): 213-222.
  • da Cunha, R., E. Jalles-Filho. 2007. The Roaring of Southern Brown Howler Monkeys (Alouatta guariba clamitans) as a Mechanism of Active Defence of Borders. Folia Primatologica, 78(4): 259–271.
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Life Expectancy

Lifespan/Longevity

Members of the genus Alouatta generally have a lifespan ranging from 15 to 20 years. Evidence suggests that males of sexually dimorphic species have shorter lifespans than females, however, there is no evidence that this occurs in brown howlers.

Range lifespan

Status: wild:
15 to 20 years.

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Lifespan, longevity, and ageing

Observations: Little is known about the longevity of these animals, but one 13.8 year old specimen was still alive in captivity (Richard Weigl 2005).
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Reproduction

Brown howlers form multi-male, multi-female groups; single-male, multi-female groups; and single-male, single-female groups. The most common group composition is single-male, multi-female with up to 10 individuals. The alpha male usually monopolizes all reproductive females and sires all young. In Primates where males outnumber females, male-male competition for resources and mates is intense, which may lead to sexual dimorphism and polygny. Adult males disperse from their natal group and must compete with alpha males to gain acceptance into a new social group.

Extra group copulations are less frequent in Alouatta relative to other Primates. After male solicitation, the female moves towards the male and performs rhythmic tongue movements. Shortly after, copulation takes place and lasts about one minute. Sometimes genital inspection also occurs. Often, female brown howlers initiate extra-group copulations and are more prone to do so in multi-male groups. Members of the female's group are indifferent to any extra group copulations that she may perform.

Mating System: monogamous ; polyandrous ; polygynous ; polygynandrous (promiscuous)

Brown howlers are year-round breeders. Their folivorous diet may account for the ability to breed year-round, as mature leaves are available throughout the year and provide a relatively stable source of energy. Rubbing behavior is well documented in several members of Primates and serves multiple functions. Adult male brown howlers exhibit extreme rubbing behavior as a marker of dominance and reproductive status. Status-based differences in rubbing behavior are also observed among female brown howlers. Rubbing plays an important role in intersexual and intrasexual dominance interactions and in aggressive and territorial behavior. Females reach adulthood at approximately 3.6 years and males at approximately 5 years.

Breeding interval: Females can breed once every 22 months

Breeding season: Brown howlers are year-round breeders

Average number of offspring: 1.

Average gestation period: 6 months.

Average weaning age: 12 months.

Average age at sexual or reproductive maturity (female): 43 months.

Average age at sexual or reproductive maturity (male): 61 months.

Key Reproductive Features: iteroparous ; year-round breeding ; gonochoric/gonochoristic/dioecious (sexes separate); viviparous

Like most primates, brown howlers have altricial young with extended periods of juvenile development. As is the case with most polygynous species, maternal investment is high in this species. Gestation last for approximately 6 months and young are usually weaned by 1 year old. Young begin to explore their environment independent of their mother at five months old. Males exhibit minimal paternal investment, and allomaternal care is rare in brown howlers.

Parental Investment: altricial ; female parental care ; pre-fertilization (Provisioning, Protecting: Female); pre-hatching/birth (Provisioning: Female, Protecting: Female); pre-weaning/fledging (Provisioning: Female, Protecting: Female); pre-independence (Protecting: Female); post-independence association with parents; extended period of juvenile learning

  • Hirano, Z., I. Correa, D. De Oliveira. 2008. Contexts of Rubbing Behavior in Alouatta guariba clamitans: A Scent-Marking Role?. American Journal of Primatology, 70(6): 575-583.
  • Miranda, J., L. Aguiar, G. Ludwig, R. Moro-Rios, F. Passos. 2005. The first seven months of an infant Alouatta guariba (Humboldt) (Primates, Atelidae): Interactions and the development of behavioral patterns. Rev. Bras. Zool., 22(4): 1191-1195.
  • Miranda, J., I. Bernardi, K. Abreu, F. Passos. 2005. Predation on Alouatta guariba Cabrera (Primates, Atelidae) by Leopardus pardalis (Linnaeus) (Carnivora, Felidae). Rev. Bras. Zool., 22(3): 793-795.
  • Miranda, J., I. Bernardi, R. Moro-Rios, L. Aguiar, G. Ludwig, F. Passos. 2004. Social structure of Alouatta guariba clamitans: a group with a dominant female. Neotropical Primates, 12(3): 135-138.
  • Pinto, L., C. Costa, K. Strier, G. da Fonseca. 1993. Habitat, Density and Group Size of Primates in a Brazilian Tropical Forest. Folia Primatologica, 61(3): 135-143.
  • Strier, K., S. Mendes, R. Santos. 2001. Timing of Births in Sympatic Brown Howler Monkeys (Alouatta fusca calmitans) and Northern Muriquis (Brachyteles arachnoides hypoxanthus). American Journal of Primatology, 55: 87-100.
  • de Souza Fialho, M., E. Setz. 2007. Extragroup Copulations Among Brown Howler Monkeys in Southern Brazil. Neotropical Primates, 14(1): 28-30.
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Conservation

Conservation Status

IUCN Red List Assessment


Red List Category
LC
Least Concern

Red List Criteria

Version
3.1

Year Assessed
2008

Assessor/s
Mendes, S.L., Rylands. A.B., Kierulff, M.C.M. & de Oliveira, M.M.

Reviewer/s
Mittermeier, R.A. & Rylands, A.B. (Primate Red List Authority)

Contributor/s

Justification
The species is listed as Least Concern because, although it occurs in the Atlantic Forest of Brazil, a region with a high rate of historical forest loss, it remains widely distributed, is present in many protected areas, and is not declining at a rate sufficient to qualify for a threat category.

History
  • 2003
    Near Threatened
  • 2003
    Near Threatened
    (IUCN 2003)
  • 2000
    Vulnerable
  • 1996
    Vulnerable
  • 1996
    Vulnerable
  • 1994
    Vulnerable
    (Groombridge 1994)
  • 1990
    Vulnerable
    (IUCN 1990)
  • 1988
    Indeterminate
    (IUCN Conservation Monitoring Centre 1988)
  • 1986
    Indeterminate
    (IUCN Conservation Monitoring Centre 1986)
  • 1982
    Indeterminate
    (Thornback and Jenkins 1982)
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On the IUCN's Red List of Threatened Species, brown howlers are listed as near threatened. However, the northern brown howler subspecies, A. guariba guariba, is listed as critically endangered. Alouatta species are relatively well adapted for surviving in small, isolated parts of the forest due to their relatively small home ranges. Despite this, habitat fragmentation due to deforestation and development in south-eastern Brazil and north-eastern Argentina is the major factors impeding the persistence of this species. The Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) lists brown howlers under Appendix II.

US Federal List: no special status

CITES: appendix ii

IUCN Red List of Threatened Species: least concern

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Status

Classified as Least Concern (LC) on the IUCN Red List (1), and listed on Appendix II of CITES (4). Two subspecies are recognised: the northern brown howler monkey (Alouatta guariba guariba) is classified as Critically Endangered (CR) and the southern brown howler monkey (Alouatta guariba clamitans) is classified as Least Concern (LC) on the IUCN Red List (1).
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Population

Population
There have been a fair number of population estimates thorughout the range of this species. Most of them in very small forest fragments. González-Solís et al. (2001) provide a recent summary. They list 11 sites (forests) where brown howlers were counted, ranging from from 50 ha to 100,000 ha. Densities can be very high. When not hunted, densities can vary in even very small forests due to their folivory and dietary flexibility. In the 50 ha site (Lageadinho, São Paulo) group size was 6-12, and the density 98 individuals/km² (Torres de Assumpção 1983). Chiarello (1993) recorded a density of 177 individuals/km² at the Santa Genebre Reserve (259 ha), São Paulo. Estimates of densities at the Caratinga Biological Statiion (survey area ranging from 570 to 800 ha), Minas Gerais, have varied from 92 to 149 individuals/km² (Mendes 1985, 1989; Hirsch 1995). Lower densities, 10.1 individuals/km², were recorded in the Augusto Ruschi Biological Reserve (4,000 ha), Espírito Santo, by Pinto et al. (1993). Hirsch (1995) estimated densities of 1.8 to 49.0 individuals/km² in the Rio Doce State Park (32,210 ha), Minas Gerais. González-Solís et al. (2001) estimated a density of 0.79 individuals/km² in the Serra do Paranapiacaba, in four contiguous protected areas in the state of São Paulo totalling 140,000 ha (the state parks of Intervales, Turístico Alto Ribeira and Carlos Botelho, and the Xitué State Ecological Station). Surveys by Chiarello (1995) in the Linhares Forest Reserve, Espírito Santo failed to register howlers even though they were present. In later surveys in the same reserve, Chiarello (1999) recorded an encounter rate of 0.15 groups/10 km. Schneider and Marques (1999) estimated a density of 92-125 individuals/km² in the southern part of the range of this species, in mixed broadleaf/Araucaria forest in the Aracuri-Esmeralda Ecological Station. Buss (2001) estimated 65 to 85 individuals/km² in the Itapuã State Park.

Note that there have been quite a number of behavioural-ecological field studies of this species, and a number of density estimates available in the literature are a result of these studies. The study sites chosen were those where howler monkeys were found to be numerous and visible, so these high densities are undoubteldy at the top end of the densities possible for this species and do not reflect a situation typical of the entire range of the species. Where they are hunted they will occur in very much lower numbers or not at all. In some areas they are scarce even though hunting is minimal or absent (for example, the Rio Doce State Park, or the Augusto Ruschi Biological Station). The explanation for low population densities in these cases is generally sought in disease epidemics, especially yellow fever.

In Misiones, Argentina, densities of both A. guariba and A. caraya are extremely low probably as a result of the dramatic habitat fragmentation suffered in the last few decades, and of an older yellow fever outbreak that occurred in 1966.

Population Trend
Decreasing
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Threats

Major Threats
Widespread forest loss and fragmentation throughout its range, hunting, and disease epidemics are the main threats. However, the species is able to survive in even quite small forest fragments if there is no hunting. Selective logging for prized Araucaria pine is a threat in the south of its range. Mortality has also been reported due to electrocution from power lines, mainly in the small populations surviving in urban parks such as Lami Municipal Reserve, Porto Alegre (Lokschin et al. 2007).
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Although the IUCN Red List classifies this species is Near Threatened (NT) overall, the nominate subspecies, the northern brown howling monkey (Alouatta guariba guariba), is classified as Critically Endangered (1). The species' populations are extremely fragmented and reduced due to habitat destruction and development in the coastal forests of south-eastern Brazil and north-eastern Argentina (1) (3). Unlike many other primates, members of this genus are actually better able to survive in small isolated parts of the forest because they do not require large home ranges (1) (5). Habitat destruction and development in this part of the world does not seem to be slowing down and it is feared that this primate and many others will suffer in due course (2).
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Management

Conservation Actions

Conservation Actions
This species is present in a number of protected areas:

Argentina
Cruce Caballero Provincial park (435 ha) (at least two groups, Di Bitteti et al. 1994; Parera 2002)
Urugua-í Provincial Park (Parera 2002)
Piñalito Natural Reserve (3,796 ha) (Parera 2002). (A. caraya also occurs in this park, between the Rios Uruguai and Paraná, and hybrids have been recorded there (Di Bitteti 2005). Di Bitetti (2005) suggested A. caraya was replacing A. guariba in ths region due to forest destruction and degradation).

Brazil

Espírito Santo
Linhares Forest Reserve (Companhia Vale do Rio Doce) (22,000 ha) (Mendes 1991; Chiarello 1995).
Augusto Ruschi Biological Reserve (3,572 ha) (Mendes, 1991; Pinto et al. 1993)
Sooretama Biological Reserve (27,943 ha) (rare, Chiarello 1999)
Córrego Grande Biological Station (1,489 ha)
Pedra Azul State Biological Reserve (1,200 ha) (Mendes 1991)
Duas Bocas State Biological Reserve (2,910 ha) (Mendes 1991)
Fazenda Montes Verdes Forest Reserve (1,500 ha) (Mendes 1991)
Santa Lúcia Biological Station (400 ha) (Mendes 1991)
São Lourenço Biological Station (22 ha) (Mendes 1991)

Minas Gerais
Caparaó National Park (across the Espírito Santo border) (31,853 ha)
Rio Doce State Park (35.973 ha) (Stallings and Robinson 1991; Hirsch 1995)
Serra do Brigadeiro State Park (13,210 ha) (Cosenza 1993)
Ibitipoca State Park (1,488 ha) (Hirsch et al. 1994)
Caratinga Biological Station RPPN Feliciano Abdala (Mendes 1985, 1989)

Paraná
Ilha Grande National Park (108,166 ha) (Aguiar et al. 2007)
Ilhas e Várzeas do Rio Paraná Environmental Protection Area (1,003,059 ha) (Aguiar et al. 2007)

Rio de Janeiro
Serra dos Órgãos National Park (10,527 ha)
Serra da Bocaina National Park (across border with São Paulo) (98,115 ha)
Itatiaia National Park (28,155 ha) (Diblasi-Filho and Borsoi Jr. 1983)
Tinguá Biologica Reserve (24.902 ha)
Poço das Antas Biological Reserve (5,065 ha)
Desengano State Park (22,500 ha)
Floresta da Cicuta State Area of Outstanding Ecological Interest (144 ha)

São Paulo
Turístico Alto Ribeira State Park (36,712 ha) (González-Solís et al. 2001)
Carlos Botelho State Park (37,644 ha) (González-Solís et al. 2001)
Morro do Diabo State Park (Coimbra Filho 1976b)
Serra do Mar State Park
Cantareira State Park (7,000 ha) (Cordeiro da Silva 1981; Oliveira and Ades 1993)
Paranapiacaba State Biological Reserve (336 ha)
Juréia-Itatins State Ecological Station (79,270 ha)
Xitué State Ecological Station (González-Solís et al. 2001)

Rio Grande do Sul
Aparados da Serra National Park (13,081 ha)
Itapuã State Park (5,566 ha) (Prates et al. 1990; Buss 2001; Marques 2003)
Espigão Alto State Park (1,319 ha) (Marques 2003)
Rondinha State Park (1,000 ha) (Marques 2003)
Turvo State Park (17,491 ha) (Marques 2003)
Serra Geral State Biological Reserve (4,846 ha) (Marques 2003)
Ibicuí-mirim Biological Reserve (598 ha) (Marques 2003)
Aracuri-Esmeralda Ecological Station (277 ha) (Marques 2003)
Lami Municipal Biological Reserve (Marques 2003)
São Francisco de Paula National Forest (1,607 ha) (Marques 2003)
Parque do Morro do Osso (Marques 2003)
Rota do Sol Environmental Protection Area (52,535 ha) (Marques 2003)

Argentina
Cruce Caballero Provincial park (435 ha) (at least two groups, Di Bitteti et al. 1994; Parera 2002)
Urugua-í Provincial Park (Parera 2002)
Piñalito Natural Reserve (Parera 2002). (A. caraya also occurs in this park, between the Rios Uruguai and Paraná, and hybrids have been recorded there [Di Bitteti 2005]. Di Bitetti (2005) suggested A. caraya was replacing A. guariba in ths region due to forest destruction and degradation).

It is listed on Appendix II of CITES.
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Conservation

Brown howling monkeys benefit from habitat protection in at least 10 different protected areas in Brazil (3). They are also in the 958 hectare sanctuary of Montes Carlos which was first bought by Feliciano Miguel Abdala for a farm in 1944 (7). Abdala was fascinated by the forest's wildlife and understood that, by trapping humidity, the forest helped to nurture his crops. Abdala therefore conserved large areas of the forest on his property and, encouraged by the World Wildlife Fund (WWF) and scientists, also provided land to build the Caratinga Biological Station in 1983. Since then the reserve has hosted dozens of Brazilian and international researchers, and following Abdala's death in 2000, was established as the Feliciano Miguel Abdala Private Natural Heritage Reserve (7). Conservation International has provided technical and financial assistance, as well as training and equipment, and is now working with local Non Governmental Organisations (NGOs), government officials and private landowners to protect more forest fragments and link them into conservation corridors in this part of the state of Minas Gerais forest zone (7). It is certainly hoped that these positive measures will protect the brown howling monkey and other wildlife of this region for the future (2).
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Relevance to Humans and Ecosystems

Benefits

Economic Importance for Humans: Negative

Howlers are potential reservoirs for human disease such as yellow fever and giardia. Nearly 15% of the rural human population in Latin America is affected by Giardia. The increased prevalence of this protozoa in howler populations (e.g., black howler monkeys) is symptomatic of increased contact with livestock and humans. Two yellow fever outbreaks in howler monkeys in northeastern Argentina seriously affected populations of southern brown howlers. In October 2008, 59 howlers were found dead in the Misiones province of Argentina, which prompted a human vaccination campaign in the area. Brown howlers also carry diseases that infect domestic livestock.

Negative Impacts: injures humans (carries human disease); causes or carries domestic animal disease

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Economic Importance for Humans: Positive

Members of the genus Alouatta are important biological indicators to overall ecosystem health and alert humans of potential epidemics. Brown howlers are hunted for meat in some human populations.

Positive Impacts: food

  • Horwich, R. 1998. Effective Solutions for Howler Conservation. International Journal of Primatology, 19(3): 579-598.
  • Kowalewski, M., J. Salzer, J. Deutsch, M. Rano, M. Kuhlenschmidt, T. Gillespie. 2011. Black and Gold Howler Monkeys (Alouatta caraya) as Sentinels of Ecosystem Health: Patterns of Zoonotic Protozoa Infection Relative to Degree of Human–Primate Contact. American Journal of Primatology, 73: 75-83.
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Wikipedia

Brown howler

The brown howler (Alouatta guariba), also known as brown howling monkey, is a species of howler monkey, a type of New World monkey that lives in forests in southeastern Brazil and far northeastern Argentina (Misiones).[1][2] It lives in groups of two to 11 individuals.[3] Despite the name "brown howler", it is notably variable in colour, with some individuals appearing largely reddish-orange or black.[4]

The two subspecies are:[1]

References

  1. ^ a b c Groves, C. P. (2005). Wilson, D. E.; Reeder, D. M. eds. Mammal Species of the World (3rd ed.). Baltimore: Johns Hopkins University Press. pp. 149. OCLC 62265494. ISBN 0-801-88221-4. http://www.bucknell.edu/msw3/browse.asp?id=12100380.
  2. ^ a b Mendes, S. L., Rylands, A. B., Kierulff, M. C. M. & de Oliveira, M. M. (2008). "Alouatta guariba". IUCN Red List of Threatened Species. Version 2011.2. International Union for Conservation of Nature. http://www.iucnredlist.org/apps/redlist/details/39916. Retrieved 19 January 2012.
  3. ^ Louise Emmons and Francois Feer (1997). Neotropical Rainforest Mammals.
  4. ^ Gregorin, R. (2006). (Portuguese) Taxonomia e variação geográfica das espécies do gênero Alouatta Lacépède (Primates, Atelidae) no Brasil. Rev. Bras. Zool. 23(1).
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