Howler monkeys[1]
Brown howler monkey
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Animalia
Phylum: Chordata
Class: Mammalia
Order: Primates
Suborder: Haplorhini
Infraorder: Simiiformes
Family: Atelidae
Subfamily: Alouattinae
Trouessart, 1897 (1825)
Genus: Alouatta
Lacepede, 1799
Type species
Simia belzebul
Linnaeus, 1766
Species

See text

Alouatta distribution
Synonyms
  • Mycetes Illiger, 1811
  • Stentor É. Geoffroy, 1812

Howler monkeys (genus Alouatta, monotypic in subfamily Alouattinae) are the most widespread primate genus in the Neotropics and are among the largest of the platyrrhines along with the muriquis (Brachyteles), the spider monkeys (Ateles) and woolly monkeys (Lagotrix). The monkeys are native to South and Central American forests. They are famous for their loud howls, which can be heard up to three miles away through dense rain forest.[2] Fifteen species are recognized. Previously classified in the family Cebidae, they are now placed in the family Atelidae. They are primarily folivores but also significant frugivores, acting as seed dispersal agents through their digestive system and their locomotion. Threats include human predation, habitat destruction, illegal wildlife trade, and capture for pets or zoo animals.

Classification

GroupImageScientific nameSubspeciesDistribution
A. palliata group Coiba Island howler, Alouatta coibensis Panama.
Mantled howler, Alouatta palliata Colombia, Costa Rica, Ecuador, Guatemala, Honduras, Mexico, Nicaragua, Panama and Peru
Guatemalan black howler, Alouatta pigra Belize, Guatemala and Mexico
A. seniculus group Ursine howler, Alouatta arctoidea Venezuela and possibly Colombia
Red-handed howler, Alouatta belzebul Brazil
Spix's red-handed howler, Alouatta discolor Brazil
Brown howler, Alouatta guariba southeastern Brazil and far northeastern Argentina (Misiones)
Juruá red howler, Alouatta juara Peru and Brazil.
Guyanan red howler, Alouatta macconnelli Suriname, Guyana, Trinidad, French Guiana, Venezuela and Brazil.
Amazon black howler, Alouatta nigerrima Brazil
Purus red howler, Alouatta puruensis
  • Alouatta puruensis amazonica
  • Alouatta puruensis arctoidea
  • Alouatta puruensis insulanus
  • Alouatta puruensis juara
  • Alouatta puruensis macconnelli
  • Alouatta puruensis puruensis
  • Alouatta puruensis sara
  • Alouatta puruensis seniculus
  • Alouatta puruensis stramineus
 Brazil, Peru and north of Bolivia.
Bolivian red howler, Alouatta sara Bolivia.
Venezuelan red howler, Alouatta seniculus Venezuela, Colombia, Ecuador, Peru and Brazil.
Maranhão red-handed howler, Alouatta ululata Brazil
A. caraya group Black howler, Alouatta caraya Paraguay, southern Brazil, eastern Bolivia, northern Argentina, and Uruguay

Anatomy and physiology

Male mantled howler

Howler monkeys have short snouts and wide-set, round nostrils. Their noses are very keen, and they can smell out food (primarily fruit and nuts) up to 2 km away. Their noses are usually roundish snout-type, and the nostrils have many sensory hairs growing from the interior. They range in size from 56 to 92 cm (22 to 36 in), excluding their tails, which can be equally long; in fact in some cases the tail has been found to be almost five times the body length. This is a prime characteristic. Like many New World monkeys, they have prehensile tails, which they use while picking fruit and nuts from trees. Unlike other New World monkeys, both male and female howler monkeys have trichromatic color vision.[3] This has evolved independently from other New World monkeys due to gene duplication.[4] They have lifespans of 15 to 20 years. Howler species are dimorphic and can also be dichromatic (i.e. Alouatta caraya). Males are typically 1.5 to 2.0 kg heavier than females.

Skull

Males experience an evolutionary trade off between investments in precopulatory traits, larger hyoids but smaller testes, or post-copulatory traits, larger testes and smaller hyoids.The hyoid of Alouatta is pneumatized, one of the few cases of postcranial pneumaticity outside the Saurischia. The volume of the hyoid of male howler monkeys is negatively correlated with the dimensions of their testes, and with the number of males per group. Larger hyoids decrease space between formant, and offers impression of larger body size.[5] They have a flat cranial shape due to a folivorous diet and an advanced vocal system. Their brain growth is posterior rather than superior or inferior as in other platyrrhines.[6]

Locomotion

Howler monkeys generally move quadrupedally on the tops of branches, usually grasping a branch with at least two hands or one hand and the tail at all times. Their strong prehensile tails are able to support their entire body weight. Fully grown adult howler monkeys do not often rely on their tails for full-body support, but juveniles do so more frequently. A significant amount of their travel is done through the ground, with sitting and resting being their most frequent postures.[7]

Behaviour

A Bolivian red howler (Alouatta sara)

Social systems


Most howler species live in groups of six to 15 animals, with one to three adult males and multiple females. Mantled howler monkeys are an exception, commonly living in groups of 15 to 20 individuals with more than three adult males. The number of males in a given group is inversely correlated with the size of their hyoids and is positively correlated with testes size.

A Red Howler with child in Monteverde Cloud Forest Biological Reserve

This results in two distinct groups, wherein one male with a larger hyoid and smaller testes copulates exclusively with a group of females, suggesting precopulatory vocal competition. The other group has more males, which have smaller hyoids, and larger testes. The larger the number of males, the smaller the hyoid, and the larger the testes.[5] Female howler monkeys breed with multiple males within their group, with males in neighboring groups, and with solitary males. Central males tie up fellowship with cycling females.[8] Unlike most New World monkeys, in which one sex remains in natal groups, juveniles of both sexes emigrate from their natal groups,[9] such that howler monkeys could spend the majority of their adult lives in association with unrelated monkeys.

Physical fighting among group members is infrequent and generally of short duration, but serious injuries can result. Both males and females rarely fight with each other, but physical aggression is even more rare between sexes.[9][10] Group size varies by species and by location, with an approximate ratio of one male to four females.[9]

Communication

A pair of black howler monkeys (Alouatta caraya) vocalising

As their name suggests, vocal communication forms an important part of their social behavior. They each have an enlarged basihyal or hyoid bone, which helps them make their loud vocalizations. Group males generally call at dawn and dusk, as well as interspersed times throughout the day. Their main vocals consist of loud, deep, guttural growls or "howls". Howler monkeys are widely considered to be the loudest land animals. According to Guinness Book of World Records, their vocalizations can be heard clearly for 3 mi (4.8 km).[11] The function of howling is thought to relate to intergroup spacing and territory protection, as well as possibly to mate-guarding. Howlers call usually when they are in areas with major feeding sites, which in some sort lead to advertise major feeding sites and their willingness to defend locally available fruit trees. Black howler monkeys incorporate information on resource availability along with neighbors’ current location. And the abundance of flowers are found to be an important factor that influenced behavior. Neighbors are more likely to move towards these calls when resource are scarce, and the reverse is true.[12]

Diet and feeding

An ursine howler

These large and slow-moving monkeys are the only folivores of the New World monkeys. Howlers eat mainly top canopy leaves, together with fruit, buds, flowers, and nuts. They need to be careful not to eat too many leaves of certain species in one sitting, as some contain toxins that can poison them.[13] Howler monkeys are also known to occasionally raid birds' nests and chicken coops and consume the eggs.[14] When in smaller groups (up to twelve individuals) and low rainfall (up to 2,200 mm (87 in)), they are more frugivorous. In larger groups and increased rainfall, frugivory decreases as a result of competition and fast food depletion.[15] As they digest fruit, more than 90% of the fruits' seeds are excreted without damage, which results in seed dispersal and distribution in tropical forests.[16]

Sleeping

Howlers use the upper-middle part of their sleeping tree and use large branches on 70% of nights which potentially allow for grouped sleeping or for resistance to weather conditions and risk of branch breaking. Their sleeping sites are usually close to morning feeding sites.[17]

Relationship with humans

While they are not usually aggressive, brown howler monkeys do not take well to captivity and are of bad-tempered and unfriendly disposition. However, the black howler monkey (Alouatta caraya) is a relatively common pet in contemporary Argentina due to its gentle nature (in comparison to the capuchin monkey's aggressive tendencies), in spite of its lesser intelligence, as well as the liabilities of the size of its droppings and the male monkey’s loud vocalizations.

John Lloyd Stephens described the howler monkeys at the Maya ruins of Copán as "grave and solemn, almost emotionally wounded, as if officiating as the guardians of consecrated ground". To the Mayas of the Classic period, they were the divine patrons of the artisans, especially scribes and sculptors. They were seen as gods in some tribes, and the long, sleek tail was worshipped for its beauty. Copán, in particular, is famous for its representations of howler monkey gods. Two howler monkey brothers play a role in the myth of the Maya Hero Twins included in the Popol Vuh, a widely feared tale of soul and passion.

References

  1. ↑ 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. pp. 148–152. ISBN 0-801-88221-4. OCLC 62265494.
  2. ↑ "Black howler monkey". Smithsonian's National Zoo. 25 April 2016. Retrieved 30 March 2023.
  3. ↑ Jacobs, G. H.; Neitz, M.; Deegan, J. F.; Neitz, J. (1996). "Trichromatic colour vision in New World monkeys". Nature. 382 (6587): 156–158. Bibcode:1996Natur.382..156J. doi:10.1038/382156a0. PMID 8700203. S2CID 4305822.
  4. ↑ Lucas, P. W.; N. J. Dominy (2003). "Evolution and function of routine trichromatic vision in primates". Evolution. 57 (11): 2636–43. doi:10.1554/03-168. PMID 14686538.
  5. 1 2 Dunn, Jacob C.; Halenar, Lauren B.; Davies, Thomas G.; Cristobal-Azkarate, Jurgi; Reby, David; Sykes, Dan; Dengg, Sabine; Fitch, W. Tecumseh; Knapp, Leslie A. (2 November 2015). "Evolutionary Trade-Off between Vocal Tract and Testes Dimensions in Howler Monkeys". Current Biology. 25 (21): 2839–2844. doi:10.1016/j.cub.2015.09.029. ISSN 0960-9822. PMC 4635310. PMID 26592343.
  6. ↑ Fiorenza, Luca; Bruner, Emiliano (2018). "Cranial shape variation in adult howler monkeys(Alouatta seniculus)". American Journal of Primatology. 80 (1): e22729. doi:10.1002/ajp.22729. PMID 29206291. S2CID 29382338.
  7. ↑ Ybarra, Miguel A. Schön (1984). "Locomotion and postures of red howlers in a deciduous forest‐savanna interface". American Journal of Physical Anthropology. 63 (1): 65–76. doi:10.1002/ajpa.1330630109. PMID 6703035.
  8. ↑ Kowalewski, Martín M; Garber, Paul A; Cortés-Ortiz, Liliana; Urbani, Bernardo; Youlato, Dionisios (2014). Howler monkeys: behavior, ecology, and conservation. Springer. pp. 10–11. ISBN 9781493919604.
  9. 1 2 3 Sussman, R. (July 2003). Primate Ecology and Social Structure, Vol. 2: New World Monkeys, Revised First Edition. Pearson Prentice Hall. pp. 142–145. ISBN 978-0-536-74364-0.
  10. ↑ Crockett (2 October 1997). "Family Feuds". In Ciochon, R. L.; Nisbett, R. A. (eds.). Primate Anthology, The: Essays on Primate Behavior, Ecology and Conservation from Natural History. Prentice Hall. p. 32. ISBN 978-0-13-613845-7.
  11. ↑ "Black howler monkey". Smithsonian’s National Zoo & Conservation Biology Institute. 4 April 2016. Retrieved 12 February 2019.
  12. ↑ Van Belle, Sarie; Estrada, Alejandro (1 April 2020). "The Influence of Loud Calls on Intergroup Spacing Mechanism in Black Howler Monkeys (Alouatta pigra)". International Journal of Primatology. 41 (2): 265–286. doi:10.1007/s10764-019-00121-x. ISSN 1573-8604. S2CID 209481526.
  13. ↑ Glander, Kenneth E. (March 1977). "Poison in a monkey's Garden of Eden" (PDF). Natural History. 86: 146–151.
  14. ↑ Walker, Matt (30 September 2009). "Monkeys 'reject vegetarianism'". Earth News. BBC. Retrieved 3 September 2022.
  15. ↑ Dias, Pedro Américo D.; Rangel-Negrín, Ariadna (2015). "Diets of Howler Monkeys". In Kowalewski, Martín M.; Garber, Paul A.; Cortés-Ortiz, Liliana; Urbani, Bernardo (eds.). Howler Monkeys: Behavior, Ecology, and Conservation. New York, NY: Springer. pp. 21–56. doi:10.1007/978-1-4939-1960-4_2. ISBN 978-1-4939-1960-4. Retrieved 30 November 2022.
  16. ↑ Cortés-Ortiz, Liliana; Rylands, Anthony B.; Mittermeier, Russell A. (2015). "The Taxonomy of Howler Monkeys: Integrating Old and New Knowledge from Morphological and Genetic Studies". In Kowalewski, Martín M.; Garber, Paul A.; Cortés-Ortiz, Liliana; Urbani, Bernardo (eds.). Howler Monkeys: Adaptive Radiation, Systematics, and Morphology. New York, NY: Springer. pp. 55–84. doi:10.1007/978-1-4939-1957-4_3. ISBN 978-1-4939-1957-4. Retrieved 2 December 2022.
  17. ↑ Brividoro, M.V; Kowalewski, M.M; Scarry, C.J (2019). "Patterns of Sleeping Site and Sleeping Tree Selection by Black-and-Gold Howler Monkeys (Alouatta caraya) in Northern Argentina". Int J Primatol. 40 (2019): 374–392. doi:10.1007/s10764-019-00094-x. S2CID 190648043.
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