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Brief Summary

Comprehensive Description

    Brown howler
    provided by wikipedia

    The brown howler (Alouatta guariba), also known as brown howler 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]

    Geographic distribution

    The brown howler lives in the Atlantic forest in South America. The region spreads through the Brazilian states of Bahia and Espirito Santo through the Rio Grande do SUl and the Misiones in the Argentine[5]

    Diet

    Brown howler monkeys are folivores and frugivorous. The diet of the brown howler monkey consists primarily of leaves and trees. Of the food sources it seems that the genera Ficus, Zanthoxylum, and, Eugenia are the most significant types consumed. Brown howler monkeys that live in higher latitudes tend to eat a lower percentage of leaves in their diet.[6] Mature leaves are less nutritious and are more fibrous, than the preferred young leaves. A typical brown howler diet will also include mature fruit, wild figs, petioles, buds, flowers, seeds, moss, stems, and twigs[2] The Atlantic forest, where brown howlers tend to live, has an increasing forest fragmentation.[5] Forest fragmentation means that there would be a decrease in potential food supplies. The brown howler’s feeding ecology, however, does not seem to be affected by the loss in habitat.[6]

    Behavior

    Howling

    Brown howler monkeys are part of the group of monkeys known for their howls/roars. Howlers are able to create such loud and specific sounds by specific body shape and structures. The larynx is enlarged and they have an enlarged open chest that creates a resonating chamber to increase the sound produced. The howlers also have specialized vocal chords to produce the specific sound.[2] The most frequent reason for the howling is for mate defense. Howling occurs most when there are both female and male howlers present. The males are the dominant group as they begin all cases of howling. Females participate in howling much less than males. Howling can also occur in groups during the dry season. It is believed that this is due to food scarcity. The brown howlers use their sounds to show ownership over certain food or territory.[7]

    Anti-predator behavior

    The black hawk eagle is a predator of the brown howler monkey. The roars of the brown howler allow the black hawk eagle to determine their location. The brown howler’s response has three parts. First, when one brown howler becomes aware of a black hawk eagle they will alarm the group and then they will immediately become silent. Next they descend in the understory of the trees, and finally they will all disperse in an organized manner. The adults will lead the young away from danger. The young are considered to be the primary target for the black hawk eagle. There is a more conservative response when adult brown howlers are without the young, and the black hawk eagle is present, thus indicating that the black hawk eagles are targeting the young howlers. When the brown howler monkey is threatened by terrestrial animals they will remain in the tree canopy and remain silent for 5–15 minutes.[8]

    Rubbing

    Brown howler monkeys rub one another for group communication. The rubbing can be used for various purposes. Males will rub their hyoid bone and sternum against each other to show agonistic and territorial signals. Males will also rub females for sexual intentions. The males are considered to be the dominant over females because they rub much more often than females. Dominate females will rub more often than non-dominate females, but still much less than males.[9]

    Reproduction

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    An adult pair and a young, also showing some of the distinct color variations in this species

    It is difficult to breed the genus Alouatta in captivity and therefore the reproduction is relatively unknown.[10] Brown howlers reproduce year round. There seems to be no correlation to birth rates in rainy or dry season or in times of increased fruit or leaves. It is thought that because the brown howler has a folivorous diet, conception is less dependent on maternal conditions.[11] The average interbirth interval (IBI) for the brown howler is 19.9 months, which is similar to other howler species. It does not seem that the sex of the infant or the number of females in the population has a significant effect on IBI. The death of an infant will shorten the mother's IBI and seems to be one of the few factors that affects IBI.[11]

    Yellow fever

    Brown howlers are highly susceptible to the yellow fever virus and have a high mortality rate when infected. When mass amounts of brown howlers are found dead it is a good inclination that there may be a yellow fever outbreak occurring. Since the brown howlers have such a high mortality rate they are not considered to maintain the virus in their population. Communities that live near the brown howler populations have previously held the belief that the brown howlers were the cause of the disease, and would kill them to stop the spread of disease. In order to protect the brown howlers the local communities should limit their killing and become vaccinated to prevent the disease from spreading.[7] The transmission of yellow fever is through mosquito vectors. In South America the known mosquito vectors of yellow fever are in the genera Haemagogus and Sabethes. In Argentina, the species that has been shown to carry the yellow fever virus (YFV) is Sabethes albiprivis.[5]

    In 2008-2009 there was a yellow fever outbreak among a brown howler study group in the protected Misiones, El Piñalito Provincial Park. The brown howler is not abundant in Argentina and any outbreak could have a detrimental effect on the population. A group of researchers have created the Brown Howler Conservation Group to continue to study and monitor yellow fever in the brown howler populations.[5]

    References

    1. ^ a b c Groves, C.P. (2005). Wilson, D.E.; Reeder, D.M., eds. Mammal Species of the World: A Taxonomic and Geographic Reference (3rd ed.). Baltimore: Johns Hopkins University Press. p. 149. ISBN 0-801-88221-4. OCLC 62265494..mw-parser-output cite.citation{font-style:inherit}.mw-parser-output q{quotes:"""""'"'"}.mw-parser-output code.cs1-code{color:inherit;background:inherit;border:inherit;padding:inherit}.mw-parser-output .cs1-lock-free a{background:url("//upload.wikimedia.org/wikipedia/commons/thumb/6/65/Lock-green.svg/9px-Lock-green.svg.png")no-repeat;background-position:right .1em center}.mw-parser-output .cs1-lock-limited a,.mw-parser-output .cs1-lock-registration a{background:url("//upload.wikimedia.org/wikipedia/commons/thumb/d/d6/Lock-gray-alt-2.svg/9px-Lock-gray-alt-2.svg.png")no-repeat;background-position:right .1em center}.mw-parser-output .cs1-lock-subscription a{background:url("//upload.wikimedia.org/wikipedia/commons/thumb/a/aa/Lock-red-alt-2.svg/9px-Lock-red-alt-2.svg.png")no-repeat;background-position:right .1em center}.mw-parser-output .cs1-subscription,.mw-parser-output .cs1-registration{color:#555}.mw-parser-output .cs1-subscription span,.mw-parser-output .cs1-registration span{border-bottom:1px dotted;cursor:help}.mw-parser-output .cs1-hidden-error{display:none;font-size:100%}.mw-parser-output .cs1-visible-error{font-size:100%}.mw-parser-output .cs1-subscription,.mw-parser-output .cs1-registration,.mw-parser-output .cs1-format{font-size:95%}.mw-parser-output .cs1-kern-left,.mw-parser-output .cs1-kern-wl-left{padding-left:0.2em}.mw-parser-output .cs1-kern-right,.mw-parser-output .cs1-kern-wl-right{padding-right:0.2em}
    2. ^ a b c d Mendes, S.L.; Rylands. A.B.; Kierulff, M.C.M. & de Oliveira, M.M. (2008). "Alouatta guariba". The IUCN Red List of Threatened Species. IUCN. 2008: e.T39916A10284881. doi:10.2305/IUCN.UK.2008.RLTS.T39916A10284881.en. Retrieved 25 December 2017.
    3. ^ Emmons, Louise & Feer, Francois (1997). Neotropical Rainforest Mammals.
    4. ^ Gregorin, R. (2006). (in Portuguese) Taxonomia e variação geográfica das espécies do gênero Alouatta Lacépède (Primates, Atelidae) no Brasil. Rev. Bras. Zool. 23(1).
    5. ^ a b c d Agostini, I., Holzmann, I., Di Bitetti, M. S., Oklander, L. I., Kowalewski, M. M., Beldomnico, P. M., . . . Miller, P. (2014). Building a Species Conservation Strategy for the brown howler monkey (Alouatta guariba clamitans) in Argentina in the context of yellow fever outbreaks. Tropical Conservation Science, 7(1), 26-34.
    6. ^ a b Chaves, Óscar M.; César Bicca-Marques, Júlio (2013). "Dietary Flexibility of the Brown Howler Monkey Throughout Its Geographic Distribution". American Journal of Primatology. 75 (1): 16–29. doi:10.1002/ajp.22075. ISSN 0275-2565. PMID 22972605.
    7. ^ a b Holzmann, Ingrid; Agostini, Ilaria; Areta, Juan Ignacio; Ferreyra, Hebe; Beldomenico, Pablo; Di Bitetti, Mario S. (2010). "Impact of yellow fever outbreaks on two howler monkey species (Alouatta guariba clamitansandA. caraya) in Misiones, Argentina". American Journal of Primatology. 72: n/a–n/a. doi:10.1002/ajp.20796. ISSN 0275-2565. PMID 20095025.
    8. ^ Miranda, João M. D.; Bernardi, Itiberê P.; Moro-Rios, Rodrigo F.; Passos, Fernando C. (2006). "Antipredator Behavior of Brown Howlers Attacked by Black Hawk-eagle in Southern Brazil". International Journal of Primatology. 27 (4): 1097–1101. doi:10.1007/s10764-006-9062-z. ISSN 0164-0291.
    9. ^ Hirano, Zelinda Maria Braga; Correa, Isabel Coelho; de Oliveira, Dilmar Alberto Gonçalves (2008). "Contexts of rubbing behavior inAlouatta guariba clamitans: a scent-marking role?". American Journal of Primatology. 70 (6): 575–583. doi:10.1002/ajp.20531. ISSN 0275-2565. PMID 18322929.
    10. ^ Veras, Mariana Matera; do Valle Marques, Karina; Miglino, Maria Angélica; Caldini, Elia Garcia (2009). "Observations on the female internal reproductive organs of the brown howler monkey (Alouatta guariba clamitans)". American Journal of Primatology. 71 (2): 145–152. doi:10.1002/ajp.20633. ISSN 0275-2565. PMID 19006197.
    11. ^ a b Strier, K. B.; Mendes, S. L.; Santos, R. R. (2001). "Timing of births in sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus)". American Journal of Primatology. 55 (2): 87–100. doi:10.1002/ajp.1042.

Distribution

    Distribution
    provided by Animal Diversity Web

    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 )

Morphology

    Morphology
    provided by Animal Diversity Web

    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

Habitat

    Habitat
    provided by Animal Diversity Web

    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

Trophic Strategy

    Trophic Strategy
    provided by Animal Diversity Web

    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 )

Associations

    Associations
    provided by Animal Diversity Web

    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:

    • 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)
    Associations
    provided by Animal Diversity Web

    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:

    • ocelot, (Leopardus pardalis)
    • black-hawk eagle, (Spizaetus tyrannus)
    • feral dogs, (Canis lupus familiaris)

Behavior

    Behavior
    provided by Animal Diversity Web

    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 ; tactile ; acoustic ; chemical

Life Expectancy

    Life Expectancy
    provided by Animal Diversity Web

    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.

Reproduction

    Reproduction
    provided by Animal Diversity Web

    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); sexual ; 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

Conservation Status

    Conservation Status
    provided by Animal Diversity Web

    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

Benefits

    Benefits
    provided by Animal Diversity Web

    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

    Benefits
    provided by Animal Diversity Web

    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

Other Articles

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