Alouatta guaribabrown howler(Also: brown howler monkey)

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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. (Chiarello, 1993; Holzmann, et al., 2010; Ingberman, et al., 2009)

Habitat

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). (Ingberman, et al., 2009; Mendes, et al., 2008; Richardson, 2005)

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. (Chiarello, 1993; Fleagle, 1988; Fortes and Bicca-Marques, 2007; Mendes, et al., 2008; Richardson, 2005; Streier, 2004)

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. (Mendes, et al., 2008)

  • Sexual Dimorphism
  • male larger
  • sexes colored or patterned differently
  • Range mass
    4 to 7 kg
    8.81 to 15.42 lb
  • Average mass
    Male: 6.7 Female: 4.3 kg
    lb
  • Range length
    56 to 92 cm
    22.05 to 36.22 in

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. (Miranda, et al., 2004; Pinto, et al., 1993; de Souza Fialho and Setz, 2007)

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. (de Souza Fialho and Setz, 2007)

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. (Hirano, et al., 2008; Miranda, et al., 2005a; Strier, et al., 2001)

  • 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

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. (Miranda, et al., 2005b; Miranda, et al., 2005a; Strier, et al., 2001)

  • 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

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. (Streier, 2004)

  • Range lifespan
    Status: wild
    15 to 20 years

Behavior

The life-history strategy of brown howlers is one of energy conservation. They spend most of their time in the upper canopy, and monkeys often travel to find seasonally available food like fruit. Brown howlers spend an average of 64% of daylight hours resting, which occurs most frequently during the middle of the day when temperatures peak. The rest of their day consists of moving (13%), feeding (18.5%), and allogrooming (2%). Adult males are the major recipients of grooming and adult females are the chief groomers. Members of the genus Alouatta move quadrupedally and do not brachiate (i.e., swing from branch to branch). Brown howlers are diurnal and territorial. (Chiarello, 1993; Chiarello, 1995a; Ingberman, et al., 2009; Streier, 2004)

  • Average territory size
    .3 km^2

Home Range

Home ranges are small, up to 31 hectares for a group of 15 to 20 individuals. Males are territorial and defend their home ranges and mates through intimidation and fighting. Brown howlers in Ilha do Cardoso State Park have lower population densities than mainland populations. In general, howler monkeys have small and widely overlapping home ranges. Alouatta guariba clamitans and Alouatta caraya hybridize in some areas, possibly due to local demography, predation risk, and habitat fragmentation. (Agostini, et al., 2008; Richardson, 2005)

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. (Chiarello, 1995b; da Cunha and Jalles-Filho, 2007)

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. (Hirano, et al., 2008)

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. (Chiarello, 1994; Martins, 2008; Martins, 2009; Richardson, 2005)

  • Plant Foods
  • leaves
  • fruit
  • flowers

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. (Bianchi and Mendes, 2007; Chiarello, 1995b; Miranda, et al., 2006)

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 (Kowalewski and Gillespie, 2009; Martins, 2006)

  • Ecosystem Impact
  • disperses seeds
Mutualist Species
  • Celtis spinosa
  • Cordia sellowiana
  • Diclidanthera
Commensal/Parasitic Species
  • mites and ticks, (Acari)
  • lice, (Pthiraptera)
  • thread worms, (Strongyloides)
  • pin worms, (Enterobideos)
  • whip worms, (Trichuris)
  • parasitic amoeba, (Entamoeba)
  • liver flukes, (Fasciola)
  • lung flukes, (Paragonimus)
  • giardia, (Giardia)

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. (Holzmann, et al., 2010; Horwich, 1998; Kowalewski, et al., 2011)

  • Positive Impacts
  • food

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. (Holzmann, et al., 2010; Kowalewski, et al., 2011)

Conservation Status

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. (Richardson, 2005)

Other Comments

Find Alouatta guariba videos, photos, and information at ARKive.

Contributors

Kendall Arslanian (author), University of Michigan-Ann Arbor, Phil Myers (editor), University of Michigan-Ann Arbor, John Berini (editor), Animal Diversity Web Staff.

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 or carries domestic animal disease

either directly causes, or indirectly transmits, a disease to a domestic animal

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

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

ranking system or pecking order among members of a long-term social group, where dominance status affects access to resources or mates

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.

female parental care

parental care is carried out by females

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).

monogamous

Having one mate at a time.

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

polyandrous

Referring to a mating system in which a female mates with several males during one breeding season (compare polygynous).

polygynandrous

the kind of polygamy in which a female pairs with several males, each of which also pairs with several different females.

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.

scent marks

communicates by producing scents from special gland(s) and placing them on a surface whether others can smell or taste them

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.

tactile

uses touch to communicate

temperate

that region of the Earth between 23.5 degrees North and 60 degrees North (between the Tropic of Cancer and the Arctic Circle) and between 23.5 degrees South and 60 degrees South (between the Tropic of Capricorn and the Antarctic Circle).

terrestrial

Living on the ground.

territorial

defends an area within the home range, occupied by a single animals or group of animals of the same species and held through overt defense, display, or advertisement

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

Agostini, I., I. Holzman, M. Bitetti. 2008. Agostini I, Holzmann I, Di Bitetti MS. 2008. Infant hybrids in a newly formed mixed species group of howler monkeys (Alouatta guariba clamitans and Alouatta caraya) in northeastern Argentina.. Primates, 49: 304-307.

Agostini, I., I. Holzman, M. Bitetti. 2010. Are Howler Monkey Species Ecologically Equivalent? Trophic Niche Overlap in Syntopic Alouatta guariba clamitans and Alouatta caraya. Journal of Primatology, 72(2): 173-186.

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.

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.

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.

Chiarello, A. 1995. Grooming in Brown Howler Monkeys, Alouatta fusca. American Journal of Primatology, 35: 73-81.

Chiarello, A. 1995. Role of Loud Calls in Brown Howlers, Alouatta fusca. American Journal of Primatology, 36(3): 213-222.

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.

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.

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.

Horwich, R. 1998. Effective Solutions for Howler Conservation. International Journal of Primatology, 19(3): 579-598.

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.

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.

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.

Martins, M. 2006. Comparative Seed Dispersal Effectiveness of Sympatric Alouatta guariba and Brachyteles arachnoides in Southeastern Brazil. Biotropica, 38(1): 57-63.

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.

Mendes, S., A. Rylands, M. Keirulff, M. de Oliveira. 2008. "Alouatta guariba" (On-line). IUCN 2010. Accessed March 20, 2011 at http://www.iucnredlist.org/apps/redlist/details/39916/0.

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.

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.

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.

Richardson, M. 2005. "Brown Howling Monkey (Alouatta guariba)" (On-line). ARKive. Accessed March 15, 2011 at http://www.arkive.org/brown-howling-monkey/alouatta-guariba/#text=Range.

Rodriguez, V., P. Dias. 2010. Effects of Habitat Fragmentation and Disturbance on Howler Monkeys: A Review. American Journal of Primatology, 72: 1-16.

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.

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.

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.

de Souza Fialho, M., E. Setz. 2007. Extragroup Copulations Among Brown Howler Monkeys in Southern Brazil. Neotropical Primates, 14(1): 28-30.