Animal Diversity Web

Diversity

Genus Alouatta belongs to family Atelidae and are among the Neotropical primates. There are currently 14 species and 7 subspecies of Alouatta recognized, though there has been some debate over taxonomy in recent years. Alouatta is often recognized by its loud and boisterous call, hence the common name of howler monkeys. Like the other members of Atelidae, Alouatta has a prehensile tail which can support individuals' body weights during foraging, feeding, and locomotion. (Di Fiore, et al., 2011; Rylands and Mittermeier, 2009)

Geographic Range

Alouatta has the largest geographic range of atelids, spanning from southeast Mexico down into central and southern North America, and even found as far south as Argentina. Of the various species, only two are found in Central America: A. palliata and A. pigra. (Di Fiore, et al., 2011; Doyle, et al., 2021; Rylands and Mittermeier, 2009)

• Biogeographic Regions
• neotropical
  • native

Habitat

Alouatta has the widest variation in habitat preference of all the Platyrrhine primates (New World monkeys). Preferred habitats range from dry, deciduous forests and riverine conditions, to wet evergreen forests with closed canopies, or even woodlands and savannah-like habitats. In recent years, much of Alouatta's habitat has been fragmented, leading to individuals being found near agricultural areas and cattle ranches. (Cortes-Ortiz, et al., 2003; Di Fiore, et al., 2011; Rylands and Mittermeier, 2009)

• Habitat Regions
• tropical
• terrestrial

• Terrestrial Biomes
• forest
• rainforest

• Other Habitat Features
• riparian

Systematic and Taxonomic History

Much of our understanding of Alouatta's taxonomy is rooted in the research of Philip Hershkovitz (1909–1997), who helped build the foundation of our modern taxonomic groupings for the infraorder Platyrrhini, to which Alouatta belongs. Some of the most recognizable traits within family Atelidae include their relatively large body size and their prehensile tails. Alouatta is the basal group within family Atelidae, separate from its three sister taxa: Ateles, Lagothhrix, and Brachyteles. This is why Alouatta is often separated into a different subfamily, Alouattinae. (Rosenberger and Strier, 1989; Rylands and Mittermeier, 2009)

The fossil record evidence shows that Alouatta may have begun to evolve away from other taxa during the middle Miocene, then spread between North and South America. According to Doyle (2021), howler monkeys were split between Mesoamerica and South America sometime around 13mya, and diversification of South American howlers occurred between 10.7 - 4.8mya (2.8mya for the Mesoamerican population). (Doyle, et al., 2021; Rosenberger and Strier, 1989)

Within genus Alouatta, there have been several changes to species and subspecies categorization. Hill (1962) categorized Alouatta into 6 species. Gregorin (2006) raised that number to 10 species, and a few years later, Cortés-Ortiz et al. (2015) classified 11 different species within Alouatta. As of 2021, as many as 14 species have been recognized, though there is still debate over whether these categories should be refined at the species or the subspecies level. Further phylogenetic analyses must be done to clearly define these taxa. (Doyle, et al., 2021)

• Synonyms

  • Mycetinae
  • Stentor

Physical Description

Alouatta exhibits sexual dimorphism in body size and coloration. Of the atelids, Alouatta has the highest level of sexual dimorphism in both weight and canine size. Males' average weight is about 7kg, with the averages from specific species ranging between 5.6kg - 11.3kg. The average body weight of an adult female is 5.5kg, with the averages from specific species ranging between 4.0kg - 6.4kg.

Alouatta are described as even-limbed, deliberately-moving quadrupeds. Their coloration ranges from black to brown, tan, and red. (Di Fiore, et al., 2011; Rosenberger and Strier, 1989)

• Other Physical Features
• endothermic
• bilateral symmetry

• Sexual Dimorphism
• male larger
• sexes colored or patterned differently

Reproduction

Both males and females in Alouatta perform mating rituals/behaviors. Sexual behaviors include tongue-flicking, displaying genitals, and initiating eye contact. Females will initiate copulations with a preferred male, which is usually the dominant, central male of the group. Males will often show aggression towards other males to protect their mates through a practice called mate guarding. Specifically, dominant males will prevent those who are not a part of the social group from copulating with the receptive females. Females have been observed soliciting lower-ranking males around their periovulatory period, possibly to confuse the paternity of the offspring. (Van Belle, et al., 2009)

• Mating System
• polygynandrous (promiscuous)

Most species in Alouatta do not have a birthing season; however, some give birth in the dry season. When their preferred foods such as young leaves are abundant, species such as A. caraya will often not exhibit seasonality. Those that live in temporally seasonal regions will display more birthing seasonality, suggesting that giving birth is linked to the abundance of food. (Di Fiore, et al., 2011; Rylands and Mittermeier, 2009)

The gestation period for Alouatta is estimated at 184 days, while the ovulation cycle is a range between 13-20 days. Females are usually receptive for about 2 days during their cycle, during which they will mate with their preferred partner(s) several times. Alouatta females generally have one infant per birth. Mothers will nurse for about 12 months before juveniles are fully weaned. (Di Fiore, et al., 2011; Van Belle, et al., 2009)

• Key Reproductive Features
• gonochoric/gonochoristic/dioecious (sexes separate)
• sexual

Within Alouatta, maternal care is most prominent during the first weeks of lactation, slowly decreasing as the offspring ages. Maternal care is often linked to food availability. (Dias, et al., 2018)

Both males and females leave their natal groups after reaching maturity, which occurs anywhere between 1-3 years of age. Females tend to leave before males and will often disperse farther from their natal group than males. Some may inherit breeding positions in their natal group and thus will not emigrate. Male often try to join an existing group, forcibly replacing the central male. Females have more trouble joining an existing group, so they will often establish a new group with other lone females. (Di Fiore, et al., 2011)

• Parental Investment
• female parental care

Lifespan/Longevity

The average lifespan of Alouatta is estimated at around 16 years for females and 17 years for males, with a maximum lifespan of about 20 years. (Di Fiore, et al., 2011)

Behavior

Alouatta, like many primates, is fairly social. Typical group sizes range from as little as 6 individuals to groups of 10-15. However, some groups of A. palliata have been reported to be as large as 40 individuals. Most groups typically consist of several adult females and one adult male, though there can be up to three males. In the larger groups found in A. palliata, there are usually 3 adult males and 9 or more adult females. The home ranges for these groups are anywhere between 8-60 hectares, averaging at around 28 hectares of land. (Di Fiore, et al., 2011; Rosenberger and Strier, 1989)

Dominance hierarchies for both males and females have been recorded within social groups. For A. palliata males, rank is often associated with age, with the youngest holding the highest rank. Affiliation between group members is usually weak, along with intrasexual relationships. When grooming behavior is reported, it is most often between a male and a female. (Di Fiore, et al., 2011)

Alouatta spend most of their day (~50%) resting and sleeping, conserving their energy between foraging bouts. They are exclusively arboreal animals, spending all their time in the trees and preferring the upper canopies. (Di Fiore, et al., 2011; Rylands and Mittermeier, 2009)

• Key Behaviors
• arboreal
• diurnal
• motile
• social
• dominance hierarchies

Communication and Perception

Alouatta communicate with each other through a variety of vocalizations and calls. Individuals in Alouatta can produce loud calls because of their throat anatomy, which includes a large hyoid that sits fairly high in the neck. Vocalizations can help communicate in situations such as an infant cawing to gain the attention of its mother (A. palliata), or a cry when an individual is separated from the group. In A. caraya, a prominent moo call appears to be used when individuals are attempting to reconnect with their group, such as when they are separated while foraging. (Rosenberger and Strier, 1989; Rylands and Mittermeier, 2009)

Alouatta is unique amongst Platyrrhini members because it is the only genus where trichromacy is routinely present. Both males and females can see in trichromatic vision. This allows them to be better adapted for foraging and dietary behaviors, such as looking for brightly colored fruit. (Stoner, et al., 2005)

• Communication Channels
• visual
• tactile
• acoustic

• Other Communication Modes
• choruses

• Perception Channels
• visual
• tactile
• acoustic
• chemical

Food Habits

Alouatta has often been regarded as the most folivorous of the New World primates. They have been reported to spend as much as 70% of their time feeding on leaves. Their general diet consists of leaves, fruit, flowers, and insects and is seasonally adaptable. Although they are great generalists, Alouatta can be highly selective about what leaves they eat. They demonstrate a preference for young, immature leaves, which appear to be more nutritious, easier to digest, and can contain lower amounts of toxins. In order to digest their high fiber diet, Alouatta has a long digestive time, relying on gut bacteria to break down the food. Despite their folivorous diet, Alouatta has a relatively simple digestive system compared to many other folivorous primates, specifically the colobines of Asia and Africa. (Di Fiore, et al., 2011; Milton, 1979; Rosenberger, 1992; Rosenberger and Strier, 1989; Rylands and Mittermeier, 2009)

• Primary Diet
• herbivore
  • folivore
  • frugivore
• omnivore

Predation

The large body sizes of Alouatta helps prevent predation to some degree, but the genus still faces several predation threats. Predator groups include large cats such as jaguars, pumas, ocelots, and other mammals like tayras. Birds of prey (harpy eagles, crested eagles, black hawk-eagles, and caracaras) have also been reported to predate on Alouatta. Infants and juveniles are most susceptible to predation because of their smaller sizes. Alouatta appears to use warning signals to acknowledge the presence of a threat, and can be seen working in groups to chase away predators. (Asensio and Gomez-Marin, 2002; McKinney, 2009)

• Anti-predator Adaptations
• aposematic

• Known Predators

  • Puma concolor
  • Leopardus pardalis
  • Eira barbara
  • Harpia harpyja
  • Morphnus guianensis
  • Spizaetus tyrannus
  • Caracara plancus

Ecosystem Roles

Some of the important roles Alouatta has on their ecosystems includes pollination, seed dispersal, and forest regeneration. Alouatta actively feeds on a wide variety of vegetation, often swallowing fruit seeds whole. These seeds eventually pass through the animals' digestive system and are deposited throughout the habitat. This helps maintain forest heterogeneity by distributing different species of plants throughout the ecosystem. (Doyle, et al., 2021; Rylands and Mittermeier, 2009)

• Ecosystem Impact
• disperses seeds
• pollinates

Economic Importance for Humans: Positive

Alouatta is still being used as bushmeat in regions of the Amazon, such as in Peru and Bolivia. Alongside providing food for local communities, Alouatta can be used as an attraction for ecotourism and potentially has a role in forest regeneration via seed dispersal. (Doyle, et al., 2021; Horwich, 1998; Rylands and Mittermeier, 2009)

• Positive Impacts
• food
• ecotourism

Economic Importance for Humans: Negative

Alouatta have been reported to feed on cultivated fruits, especially when their natural diet is strained by poor food availability. However, landowners in regions with howler monkeys report that there is no production loss or lack of produce because of the monkeys' presence. Thus, the human-wildlife conflict between farmers and howler monkeys appears to be low. (Chaves and Bicca-Marques, 2017)

• Negative Impacts
• crop pest

Conservation Status

Alouatta shows a range of conservation statuses, with some such as A. macconnelli being listed as Least Concerned according to the IUCN Red List, while others are listed as Vulnerable or Endangered (i.e. A. palliata, A.guariba, and A. pigra). The main threat to the survival of howler monkeys is human disturbance. In recent years, humans have begun to encroach upon wildlife spaces, creating a variety of challenges for native species such as fragmenting habitats, reduced food availability, and therefore higher energy costs required for survival. For example, howlers must travel farther and forage longer to maintain the same degree of caloric intake, along with an increase in consumption of novel foods. (Arroyo-Rodriguez and Dias, 2010; Chaves and Bicca-Marques, 2017; Horwich, 1998; McKinney, et al., 2015; Rylands and Mittermeier, 2009)

Despite these challenges, steps are being taken to help protect howler monkeys. One such solution is the use of protected natural areas, which ensures that native populations have a place of refuge. Furthermore, Alouatta demonstrates some flexibility in food choice, such as eating cultivated fruits. These cultivated foods provide a valuable source of calories in a way that allows humans and Alouatta to share living space. Additionally, ecotourism has the potential to be an efficient resource for both conservation and economic development. Costa Rica in particular is a great example of how ecotourism, when done properly, can positively impact native wildlife species. (Chaves and Bicca-Marques, 2017; McKinney, et al., 2015)

• IUCN Red List [Link]

  Not Evaluated

Other Comments

In 1934, Clarence Raymond Carpenter conducted an extended field study on mantled howler monkeys (Alouatta palliata) in Panama, making them the first primates to undergo an extended field study in the wild. (Rylands and Mittermeier, 2009)

Contributors

Emily Dumstorff (author), Colorado State University, Audrey Bowman (editor), Colorado State University, Sydney Collins (editor), Colorado State University.

References

2021. "Alouatta" (On-line). Integrated Taxonomic Information System- Report. Accessed February 06, 2022 at https://www.itis.gov/servlet/SingleRpt/SingleRpt?search_topic=TSN&anchorLocation=SubordinateTaxa&credibilitySort=TWG%20standards%20met&rankName=ALL&search_value=572810&print_version=SCR&source=from_print#SubordinateTaxa/.

Anzures-Dadda, A., R. Manson. 2007. Patch- and landscape-scale effects on howler monkey distribution and abundance in rainforest fragments. Animal Conservation, Vol. 10(1): 69-76.

Arroyo-Rodriguez, V., P. Dias. 2010. Effects of habitat fragmentation and disturbance on howler monkeys: a review. American Journal of Primatology, Vol. 72(1): 1-16.

Asensio, N., F. Gomez-Marin. 2002. Interspecific Interaction and Predator Avoidance Behavior in Response to Tayra (Eira barbara) by Mantled Howler Monkeys (Alouatta palliata). Primates, Vol. 43(4): 339-341.

Chaves, O., J. Bicca-Marques. 2017. Crop Feeding by Brown Howlers (Alouatta guariba clamitans) in Forest Fragments: The Conservation Value of Cultivated Species. International Journal of Primatology, Vol.38(2): 263-281.

Cortes-Ortiz, L., E. Bermingham, C. Rico, E. Rodriguez-Luna, I. Sampaio, M. Ruiz-Garcia. 2003. Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta. Molecular Phylogenetics and Evolution, Vol. 26(1): 64-81.

Di Fiore, A., A. Link, C. Campbell. 2011. The Atelines: Behavioral and Socioecological Diversity in New World Monkey Radiation. Pp. 155-187 in C Campbell, A Fuentes, K MacKinnon, S Bearder, R Stumpf, eds. Primates in Perspective. New York, New York: Oxford University Press, Inc.

Dias, P., B. Cano-Huertes, A. Coyohua-Fuentes, D. Chavira-Ramírez, D. Canales-Espinosa, A. Rangel-Negrín. 2018. Maternal condition and maternal investment during lactation in mantled howler monkeys. American Journal of Physical Anthropology, Vol. 167(1): 178-184.

Doyle, E., I. Prates, I. Sampaio, C. Koiffmann, W. Silva, A. Carnaval, E. Harris. 2021. Molecular phylogenetic inference of the howler monkey radiation (Primates: Alouatta). Primates, Vol. 62(1): 177-188.

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

McKinney, T. 2009. Anthropogenic Change and Primate Predation Risk: Crested Caracaras (Caracara plancus) Attempt Predation on Mantled Howler Monkeys (Alouatta palliata). Neotropical Primates, Vol.16(1): 24-27.

McKinney, T., J. Westin, J. Serio-Silva. 2015. Anthropogenic Habitat Modification, Tourist Interactions and Crop-Raiding in Howler Monkeys. Pp. 281-311 in M Kowalewski, P Garber, L Cortes-Ortiz, B Urbani, D Youlatos, eds. Howler monkeys : behavior, ecology, and conservation. New York, New York: Springer.

Milton, K. 1979. Factors influencing leaf choice by howler monkeys: a test of some hypotheses of food selection by generalist herbivores. The American Naturalist, Vol.114 (3): 362-378.

Opazo, J., D. Wildman, T. Prychitko, R. Johnson, M. Goodman. 2006. Phylogenetic relationships and divergence times among New World monkeys (Platyrrhini, Primates). Molecular Phylogenetics and Evolution, Vol. 40 (1): 274-280.

Rosenberger, A. 1992. Evolution of feeding niches in New World monkeys. American Journal of Physical Anthropology, Vol. 88: 525-562.

Rosenberger, A., K. Strier. 1989. Adaptive radiation of the Ateline primates. Journal of Human Evolution, Vol. 18 (7): 717-750.

Rylands, A., R. Mittermeier. 2009. The diversity of the New World primates (Platyrrhini): an annotated taxonomy. Pp. 23-54 in P Garber, A Estrada, J Bicca-Marques, E Heymann, K Strier, eds. South American Primates. New York, New York: Springer.

Stoner, K., P. Riba-Hernández, P. Lucas. 2005. Comparative use of color vision for frugivory by sympatric species of platyrrhines. American Journal of Primatology, Vol 67(4): 399-409.

Van Belle, S., A. Estrada, T. Ziegler, K. Strier. 2009. Sexual behavior across ovarian cycles in wild black howler monkeys ( Alouatta pigra ): male mate guarding and female mate choice. American Journal of Primatology, Vol. 71(2): 153-164.

Wilson, D., D. Reeder. 2005. "Genus Alouatta" (On-line). Mammal Species of the World. A Taxonomic and Geographic Reference (3rd ed). Accessed February 06, 2022 at http://www.departments.bucknell.edu/biology/resources/msw3/browse.asp?id=12100374.