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Overview

Brief Summary

Biology

The mantled howler monkey is a truly arboreal species, quadrupedally walking and climbing through the canopy or suspending themselves below branches, hanging by the arms and anchoring themselves with their long tail whilst feeding (3). They often cross open areas between forest patches on the ground and are able to swim (3). They are active during the day and sleep on horizontal tree branches at night (3). This species spends much of its time foraging on leaves, fruit and flowers (5). Like all members of the genus Alouatta, the mantled howler monkey has very large salivary glands, which help it to break down the tannins in the leaves before they reach the gut (6). The mantled howler monkey lives in groups usually numbering between 10 to 20 individuals, in which a distinct social hierarchy exists. There is an alpha male who has priority access to receptive females within the group (3) (5). Females form the stable core within a group, very rarely leaving once established (5). Breeding occurs throughout the year but births are more common in late December and January (3) (5). A single young is produced after a gestation period of around six months (5) (6). The newborn infant is licked and carried by the mother (3). As it ages, the infant begins to ride around on its mother's back, grasping the base of her tail with its own (5). For the first four months of life the young monkey will not venture further than two meters away from its mother (3). Sexual maturity is reached at 36 months in females and 42 months in males (5).
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Description

Mantled howler monkeys are large, fairly stocky monkeys (5) that are totally black in colour with the exception of a fringe of long golden hairs on the flanks (3). The tail is prehensile and has a naked patch on the underside towards the tip to aid in grasping (5). The face is naked but features a beard that is longer in males than in females (5). When males reach maturity, the scrotum turns white (3). Newborns are golden brown to silvery in colour and weigh 0.4 kg (5). A range of vocalisations are produced, including barks, grunts, and woofs. The howls characteristic of this group of monkeys, and which earn this species its common name, are produced at dawn and dusk, as well as in response to disturbance (5).
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Distribution

Range Description

There are five recognized subspecies:

Alouatta palliata palliata
The range limits separating A. p. aequatorialis from A. p. palliata are not clear. Lawrence (1933) cited a specimen of A. p. palliata from Cotó, extreme western Panama, and Hill (1962, p.106) mentioned that specimens from Sevilla Island, western Panama, collected by J. H. Batty were “manifestly” A. p. palliata. Hall (1981), on the other hand, lists Sevilla Island, and Puerto Cortez, Costa Rica, as marginal records for A. p. aequatorialis. Many individuals from Panama are intermediate (Lawrence 1933). From eastern Costa Rica, at least, A. p. palliata extends through Nicaragua to northern Honduras and, according to Curdts (1993), it just extends into Guatemala to the Río Motagua and possibly along the coast a short distance to the Cabo de Tres Puntas, where it meets A. pigra. Baumgarten and Williamson (2007) found the northern most limit of A. palliata palliata in the south margin of Rio Dulce. It is not known to occur in El Salvador to the south (Burt and Stirton 1961). There are no current records of this subspecies in El Salvador, although it evidently occurred there in the past (Daugherty 1972).

Alouatta palliata mexicana
The range of A. p. mexicana extends eastward from south-eastern Mexico, provinces of Vera Cruz, Tabasco, and northern Chiapas and Oaxaca. As discussed by Smith (1970), in Tabasco A. p. mexicana meets, and is sympatric with, A. pigra in a region five miles south-east of Macuspana. García-Orduña et al. (1999) found mixed populations of the two species in small habitat fragments in Tabasco (see also Rodríguez-Luna et al. 2001). Cortés-Ortiz et al. (2003) recorded a zone of contact and possible hybridization between A. palliata mexicana and A. pigra between the ríos Grijalva and Usamacinta on the Mexico-Guatemala border. Although several published maps include its range as extending into the highlands of Chiapas and into north-central Guatemala, an ongoing study (A. Cuarón) indicates that this subspecies range is restricted to western Chiapas, central and western Tabasco, south-eastern Veracruz, and eastern Oaxaca.

Baumgarten and Williamson (2007) provide the most recent review of the limits of the distributions of Alouatta palliata and A. pigra in Central America and Mexico. They found that the highland massif of northern Central America (including the Sierra Madre de Chiapas and central highland of Guatemala) and its associated coniferous and subalpine vegetation formed a geographic barrier separating A. pigra from A. palliata, and define the southern limit of A. pigra. They discussed the two contact zones between them: the broad range of overlap north of the highland massif in Mexico over the lowlands of the states of Tabasco and Campeche, and a narrow area of contiguous, non-overlapping ranges in eastern Guatemala where the highlands extend almost to the Caribbean. In the first, the localities where parapatry has been observed include Macuspana, Tabasco (Smith 1970, Horwich and Johnson 1986), around Zapata, Tabasco (Horwich and Johnson 1986) and the northern point of the Laguna de Términos in Campeche (Serio-Silva et al. 2006). There is no geographical barrier separating the species, both occur in the same forests and on both sides of the Rio Usamacinta, for example (Cortés-Ortiz et al. 2003). In the second, the ranges are narrowly parapatric, separated by the Río Dulce and the Lago Izabal: A. palliata to the south and A. pigra to the north and west. South-west of Lake Izabal, A. pigra occurs in the highlands of the Sierra de las Minas, but not in the lowlands, occupied by A. palliata. Any past range overlap in this region will have been lost by the extensive loss of forest (the area is heavily farmed). Baumgarten (2006) found no evidence to support sympatry supposed previously by Horwich and Johnson (1986), Curdts (1993) and Silva-López et al. (1998).

Baumgarten ansd Williamson (2007) argued that A. palliata will have occurred on the Pacific side of the highland massif of northern Central America in the past. There are historical records in Mexico (Estrada and Coates-Estrada 1984), Guatemala (Handley 1950), and El Salvador (Daugherty 1972).

Alouatta palliata aequatorialis
A. p. aequatorialis occurs in Panama, from the southern limit to the range of A. p. palliata (either in western Panama or extreme eastern Costa Rica), through the Serranía del Darién (Anthony 1916, Lawrence 1933) into western Colombia, north through the basins of the Ríos Sinú and Atrato to the Caribbean coast, and south through the Serranía del Baudó (Defler 2003) and the foothills, lowlands and lower montane areas west of the Andes to the Pacific coast, through Colombia and Ecuador, just into the Tumbes and Piura region of northern Peru (Aquino and Encarnación 1994; Encarnación and Cook 1998; Tirira 2001, 2007).

Alouatta palliata coibensis
This howler monkey is known only from Coiba Island and neighbouring Jicarón, off the Pacific coast of Panama.

Alouatta palliata trabeata
This subspecies is endemic to the Azuero Peninsula, Panama (Froehlich and Froehlich 1987, Rowe 2000, Mendes-Carvajal 2005).
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Geographic Range

Mantled howler monkeys are found in southern Mexico (the states of Veracruz, Campeche, Chiapas, Oaxaca, and Tabasco), from Honduras in Central America to Colombia and western Ecuador in South America, and possibly in southern Guatemala where some unconfirmed sightings have been reported (Reid 1997, Cortes-Ortiz et al. 1996). This range includes most forest habitats that lie between sea level and 2500 meters (Reid 1997).

Biogeographic Regions: neotropical (Native )

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Historic Range:
Mexico to South America

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Range

Mantled howler monkeys occur throughout the south of Mexico, southern Guatemala extending southwards through Central America reaching the west coast of Colombia and Ecuador (3).
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Physical Description

Morphology

Physical Description

Mantled howler monkeys are large and stocky with black fur, and most individuals have long, yellow or brown fur saddles (Reid 1997, Glander 1983). Long guard hairs are present on their flanks, earning the common name "mantled" howler monkey (Glander 1983). The face is naked, black and bearded, and the prehensile tail has a naked pad on the underside near its base. Males have a prominent white scrotum, weigh 6 to 7 kg, and usually have a longer beard than female individuals (Reid 1997, Glander 1983). Adult females typically weigh 4 to 5 kg, and newborn infants weigh 0.4 kg and appear silver to golden brown (Glander 1983). Adult tail size ranges from 520 to 670 mm, and body length ranges from 380 to 580 mm (Reid 1997). The dental formula is (I 2/2, C 1/1, PM 3/3, M 3/3) X 2 = 36.

Range mass: 3 to 9 kg.

Sexual Dimorphism: male larger

Average basal metabolic rate: 11.464 W.

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Type Information

Type for Alouatta palliata
Catalog Number: USNM 79398
Collection: Smithsonian Institution, National Museum of Natural History, Department of Vertebrate Zoology, Division of Mammals
Sex/Stage: Male; Adult
Preparation: Skin; Skull
Collector(s): E. Nelson & E. Goldman
Year Collected: 1896
Locality: Minatitlan, Veracruz, Mexico, North America
Elevation (m): 30
  • Type: Merriam, C. H. 1902 Mar 22. Proceedings of the Biological Society of Washington. 15: 67.
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Type for Alouatta palliata
Catalog Number: USNM 171068
Collection: Smithsonian Institution, National Museum of Natural History, Department of Vertebrate Zoology, Division of Mammals
Sex/Stage: Male; Adult
Preparation: Skin; Skull
Collector(s): E. Goldman
Year Collected: 1911
Locality: Cerro Azul, near headwaters of Chagres River, Panama, North America
Elevation (m): 762
  • Type: Goldman, E. A. 1913 Feb 28. Smithsonian Miscellaneous Collections. 60 (22): 17.
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Ecology

Habitat

Belizean Coast Mangroves Habitat

This species is found in the Belizean coast mangroves ecoregion (part of the larger Mesoamerican Gulf-Caribbean mangroves ecoregion), extending along the Caribbean Coast from Guatemala, and encompassing the mangrove habitat along the shores of the Bahía de Annatique; this ecoregion continues along the Belizean coast up to the border with Mexico. The Belizean coast mangroves ecoregion includes the mainland coastal fringe, but is separate from the distinct ecoregion known as the Belizean reef mangroves which are separated from the mainland. This ecoregion includes the Monterrico Reserve in Guatemala, the estuarine reaches of the Monkey River and the Placencia Peninsula. The ecoregion includes the Burdon Canal Nature Reserve in Belize City, which reach contains mangrove forests and provides habitat for a gamut of avian species and threatened crocodiles.

Pygmy or scrub mangrove forests are found in certain reaches of the Belizean mangroves. In these associations individual plants seldom surpass a height of 150 centimetres, except in circumstances where the mangroves grow on depressions filled with mangrove peat. Many of the shrub-trees are over forty years old. In these pygmy mangrove areas, nutrients appear to be limiting factors, although high salinity and high calcareous substrates may be instrumental. Chief disturbance factors are due to hurricanes and lightning strikes, both capable of causing substantial mangrove treefall. In many cases a pronounced gap is formed by lightning strikes, but such forest gaps actually engender higher sapling regrowth, due to elevated sunlight levels and slightly diminished salinity in the gaps.

Chief mangrove tree species found in this ecoregion are White Mangrove (Laguncularia racemosa), Red Mangrove (Rhizophora mangle), Black Mangrove (Avicennia germinans); the Button Mangrove (Conocarpus erectus) is a related tree associate. Red mangrove tends to occupy the more seaward niches, while Black mangrove tends to occupy the more upland niches. Other plant associates occurring in this ecoregion are Dragonsblood Tree (Pterocarpus officinalis), Guiana-chestnut (Pachira aquatica) and Golden Leatherfern (Acrostichum aureum).

In addition to hydrological stabilisation leading to overall permanence of the shallow sea bottom, the Belizean coastal zone mangrove roots and seagrass blades provides abundant nutrients and shelter for a gamut of juvenile marine organisms. A notable marine mammal found in the shallow seas offshore is the threatened West Indian Manatee (Trichecus manatus), who subsists on the rich Turtle Grass (Thalassia hemprichii) stands found on the shallow sea floor.

Wood borers are generally more damaging to the mangroves than leaf herbivores. The most damaging leaf herbivores to the mangrove foliage are Lepidoptera larvae. Other prominent herbivores present in the ecoregion include the gasteropod Littorina angulifera and the Mangrove Tree Crab, Aratus pisonii.

Many avian species from further north winter in the Belizean coast mangroves, which boast availability of freshwater inflow during the dry season. Example bird species within or visiting this ecoregion include the Yucatan Parrot (Amazona xantholora), , Yucatan Jay (Cyanocorax yucatanicus), Black Catbird (Dumetella glabrirostris) and the Great Kiskadee (Pitangus sulfuratus)

Upland fauna of the ecoregion include paca (Agouti paca), coatimundi (Nasua narica),  Baird’s Tapir (Tapirus bairdii), with Black Howler Monkey (Alouatta caraya) occurring in the riverine mangroves in the Sarstoon-Temash National Park. The Mantled Howler Monkey (Alouatta palliata) can be observed along the mangrove fringes of the Monkey River mouth and other portions of this mangrove ecoregion.

Other aquatic reptiian species within the ecoregion include Morelet's Crocodile (Crocodylus moreletti), Green Turtle (Chelonia mydas), Hawksbill Sea Turtle (Eretmochelys imbricata), Loggerhead Sea Turtle (Caretta caretta), and Kemp’s Ridley (Lepidochelys kempi).

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Rio Negro-Rio San Sun Mangroves Habitat

This taxon occurs in the Rio Negro-Rio San Sun mangroves, which consists of a disjunctive coastal ecoregion in parts of Costa Rica, extending to the north slightly into Nicaragua and south marginally into Panama. Furthermore, this species is not necessarily restricted to this ecoregion. Mangroves are sparse in this ecoregion, and are chiefly found in estuarine lagoons and small patches at river mouths growing in association with certain freshwater palm species such as the Yolillo Palm (Raphia taedigera), which taxon has some saline soil tolerance, and is deemed a basic element of the mangrove forest here. These mangrove communities are also part of a mosaic of several habitats that include mixed rainforest, wooded swamps, coastal wetlands, estuarine lagoons, sand backshores and beaches, sea-grasses, and coral reefs.

The paucity of mangroves here is a result of the robust influx of freshwater to the coastline ocean zone of this ecoregion. Among the highest rates of rainfall in the world, this ecoregion receives over six metres (m) a year at the Nicaragua/ Costa Rica national border. Peak rainfall occurs in the warmest months, usually between May and September. A relatively dry season occurs from January to April, which months coincides with stronger tradewinds. Tides are semi-diurnal and have a range of less than one half metre.

Mangroves play an important role in trapping sediments from land that are detrimental to the development of both coral reefs and sea grasses that are associated with them. Mangrove species including Rhizopora mangle, Avicennia germinans, Laguncularia racemosa, Conocarpus erecta and R. harrisonii grow alone the salinity gradient in appropriate areas. Uncommon occurrences of Pelliciera rhizophorae and other plant species associated with mangroves include Leather ferns Acrostichum spp., which also invade cut-over mangrove stands and provide some protection against erosion. In this particular ecoregion, the mangroves are associated with the indicator species, freshwater palm, Raphia taedigera. Other mangrove associated species are Guiana-chestnut ( Pachira aquatica) and Dragonsblood Tree (Pterocarpus officinalis).

Reptiles include the Basilisk Lizard (Basiliscus basiliscus), Caiman (Caiman crocodilus), Green Sea Turtle (Chelonia mydas), Leatherback Turtle (Dermochelys coriacea) and Green Iguana (Iguana iguana). The beaches along the coast within this ecoregion near Tortuguero are some of the most important for nesting green turtles. The offshore seagrass beds, which are among the most extensive in the world, are a source of food and refuge for the endangered Green Sea Turtle (Chelonia mydas). Several species of frogs  of the family Dendrobatidae are found in this mangrove ecoregion as well other anuran species and some endemic salamander taxa.

Mammal species found in this highly diverse ecoregion include: Lowland Paca (Agouti paca), primates such as Mantled Howler Monkey (Alouatta palliata), Geoffrey's Spider Monkey (Ateles geoffroyi), White-faced Capuchin (Cebus capucinus), Brown-throated Sloth (Bradypus variegatus), Silky Anteater (Cyclopes didactylus) and Nine-banded Armadillo (Dasypus novemcintus).  Also found in this ecoregion are carnivores such as Ocelot (Leopardus pardalis),  Central American Otter (Lutra annectens), Jaguar (Panthera onca), Northern Racooon (Procyoon lotor), and Crab-eating Racoon (P. cancrivorus).

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Moist Pacific Coast Mangroves Habitat

This taxon occurs in the Moist Pacific Coast mangroves, an ecoregion along the Pacific coast of Costa Rica with a considerable number of embayments that provide shelter from wind and waves, thus favouring mangrove establishment. Tidal fluctuations also directly influence the mangrove ecosystem health in this zone. The Moist Pacific Coast mangroves ecoregion has a mean tidal amplitude of three and one half metres,

Many of the streams and rivers, which help create this mangrove ecoregion, flow down from the Talamanca Mountain Range. Because of the resulting high mountain sediment loading, coral reefs are sparse along the Pacific coastal zone of Central America, and thus reef zones are chiefly found offshore near islands. In this region, coral reefs are associated with the mangroves at the Isla del Caño Biological Reserve, seventeen kilometres from the mainland coast near the Térraba-Sierpe Mangrove Reserve. The Térraba-Sierpe, found at the mouths of the Térraba and Sierpe Rivers, is considered a wetland of international importance.

Because of high moisture availability, the salinity gradient is more moderate than in the more northern ecoregion such as the Southern dry Pacific Coast ecoregion. Resulting mangrove vegetation is mixed with that of marshland species such as Dragonsblood Tree (Pterocarpus officinalis), Campnosperma panamensis, Guinea Bactris (Bactris guineensis), and is adjacent to Yolillo Palm (Raphia taedigera) swamp forest, which provides shelter for White-tailed Deer (Odocoileus virginianus) and Mantled Howler Monkeys (Alouatta palliata). Mangrove tree and shrub taxa include Red Mangrove (Rhizophora mangle), Mangle Caballero (R. harrisonii) R. racemosa (up to 45 metres in canopy height), Black Mangrove (Avicennia germinans) and Mangle Salado (A. bicolor), a mangrove tree restricted to the Pacific coastline of Mesoamerica.

Two endemic birds listed by IUCN as threatened in conservation status are found in the mangroves of this ecoregion, one being the Mangrove Hummingbird (Amazilia boucardi EN), whose favourite flower is the Tea Mangrove (Pelliciera rhizophorae), the sole mangrove plant pollinated by a vertebrate. Another endemic avain species to the ecoregion is the  Yellow-billed Cotinga (Carpodectes antoniae EN).  Other birds clearly associated with the mangrove habitat include Roseate Spoonbill (Ajaia ajaja), Gray-necked Wood Rail (Aramides cajanea), Rufous-necked Wood Rail (A. axillaris), Mangrove Black-hawk (Buteogallus anthracinus subtilis),Striated Heron (Butorides striata), Muscovy Duck (Cairina moschata), Boat-billed Heron (Cochlearius cochlearius), American White Ibis (Eudocimus albus), Amazon Kingfisher (Chloroceryle amazona), Mangrove Cuckoo (Coccyzus minor), Yellow Warbler (Setophaga petechia), and Black-necked Stilt (Himantopus mexicanus VU) among other avian taxa.

Mammals although not as numerous as birds, include species such as the Lowland Paca (Agouti paca), Mantled Howler Monkey (Alouatta palliata), White-throated Capuchin (Cebus capucinus), Silky Anteater (Cyclopes didactylus), Central American Otter (Lontra longicaudis annectens), White-tailed Deer (Odocoileus virginianus), feeds on leaves within A. bicolor and L. racemosa forests. Two raccoons: Northern Raccoon (Procyon lotor) and Crab-eating Raccoon (P. cancrivorus) can be found, both on the ground and in the canopy consuming crabs and mollusks. The Mexican Collared Anteater (Tamandua mexicana) is also found in the Moist Pacific Coast mangroves.

There are a number of amphibians in the ecoregion, including the anuran taxa: Almirante Robber Frog (Craugastor talamancae); Chiriqui Glass Frog (Cochranella pulverata); Forrer's Grass Frog (Lithobates forreri), who is found along the Pacific versant, and is at the southern limit of its range in this ecoregion. Example salamanders found in the ecoregion are the Colombian Worm Salamander (Oedipina parvipes) and the Gamboa Worm Salamander (Oedipina complex), a lowland organism that is found in the northern end of its range in the ecoregion. Reptiles including the Common Basilisk Lizard (Basiliscus basiliscus), Boa Constrictor (Boa constrictor), American Crocodile (Crocodilus acutus), Spectacled Caiman (Caiman crocodilus), Black Spiny-tailed Iguana (Ctenosaura similis) and Common Green Iguana (Iguana iguana) thrive in this mangrove ecoregion.

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Mesoamerican Gulf-Caribbean Mangroves Habitat

This taxon is found in the Mesoamerican Gulf-Caribbean mangroves ecoregion, but not necessarily exclusive to this region.The Mesoamerican Gulf-Caribbean mangroves occupy a long expanse of disjunctive coastal zone along the Caribbean Sea and Gulf of Mexico for portions of Central America and Mexico. The ecoregion has a very high biodiversity and species richness of mammals, amphibians and reptiles. As with most mangrove systmems, the Mesoamerican Gulf-Caribbean ecoregion plays an important role in shoreline erosion prevention from Atlantic hurricanes and storms; in addition these mangroves are significant in their function as a nursery for coastal fishes, turtles and other marine organisms.

This disjunctive Neotropical ecoregion is comprised of elements lying along the Gulf of Mexico coastline of Mexico south of the Tampico area, and along the Caribbean Sea exposures of Belize, Honduras, Guatemala, Nicaragua, Costa Rica and Panama.There are 507 distinct vertebrate species that have been recorded in the Mesoamerican Gulf-Caribbean mangroves ecoregion.

Chief mangrove tree species found in the central portion of the ecoregion (e.g. Belize) are White Mangrove (Laguncularia racemosa), Red Mangrove (Rhizophora mangle), and Black Mangrove (Avicennia germinans); Buttonwood (Conocarpus erectus) is a related tree associate. Red mangrove tends to occupy the more seaward niches, while Black mangrove tends to dominate the more upland niches. Other plant associates occurring in this central part of the ecoregion are Swamp Caway (Pterocarpus officinalis), Provision Tree (Pachira auatica) and Marsh Fern (Acrostichum aureum).

The Mesoamerican Gulf-Caribbean mangroves ecoregion has a number of mammalian species, including: Mexican Agouti (Dasyprocta mexicana, CR); Mexican Black Howler Monkey (Alouatta pigra, EN); Baird's Tapir (Tapirus bairdii, EN); Central American Spider Monkey (Ateles geoffroyi, EN); Giant Anteater (Myrmecophaga tridactyla); Deppe's Squirrel (Sciurus deppei), who ranges from Tamaulipas, Mexico to the Atlantic versant of Costa Rica; Jaguar (Panthera onca, NT), which requires a large home range and hence would typically move between the mangroves and more upland moist forests; Margay (Leopardus wiedii, NT); Mantled Howler Monkey (Alouatta palliata); Mexican Big-eared Bat (Plecotus mexicanus, NT), a species found in the mangroves, but who mostly roosts in higher elevation caves; Central American Cacomistle (Bassariscus sumichrasti).

A number of reptiles have been recorded within the ecoregion including the Green Turtle (Chelonia mydas, EN); Hawksbill Sea Turtle (Eretmochelys imbricata, CR); Central American River Turtle (Dermatemys mawii, CR), distributed along the Atlantic drainages of southern Mexico to Guatemala; Morelets Crocodile (Crocodylus moreletii, LR/CD), a crocodile found along the mangroves of Yucatan, Belize and the Atlantic versant of Guatemala.

Some of the other reptiles found in this ecoregion are the Adorned Graceful Brown Snake (Rhadinaea decorata); Allen's Coral Snake (Micrurus alleni); Eyelash Palm Pitviper (Bothriechis schlegelii); False Fer-de-lance (Xenodon rabdocephalus); Blood Snake (Stenorrhina freminvillei); Bridled Anole (Anolis frenatus); Chocolate Anole (Anolis chocorum), found in Panamanian and Colombian lowland and mangrove subcoastal forests; Furrowed Wood Turtle (Rhinoclemmys areolata. NT); Brown Wood Turtle (LR/NT); Belize Leaf-toed Gecko (Phyllodactylus insularis), which occurs only in this ecoregion along with the Peten-Veracruz moist forests.

Salamanders found in this ecoregion are: Cukra Climbing Salamander (Bolitoglossa striatula); Rufescent Salamander (Bolitoglossa rufescens); Alta Verapaz Salamander (Bolitoglossa dofleini, NT), the largest tropical lungless salamander, whose coastal range spans Honduras, Guatemala and the Cayo District of Belize; Colombian Worm Salamander (Oedipina parvipes), which occurs from central Panama to Colombia; La Loma Salamander (Bolitoglossa colonnea), a limited range taxon occurring only in portions of Costa Rica and Panama;.Central American Worm Salamander (Oedipina elongata), who inhabits very moist habitats; Cienega Colorado Worm Salamander (Oedipina uniformis, NT), a limited range taxon found only in parts of Costa Rica and Panama, including higher elevation forests than the mangroves; Limon Worm Salamander (Oedipina alfaroi, VU), a restricted range caecilian found only on the Atlantic versant of Costa Rica and extreme northwest Panama. Caecilians found in the ecoregion are represented by: La Loma Caecilian (Dermophis parviceps), an organism found in the Atlantic versant of Panama and Costa Rica up to elevation 1200 metres

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Habitat and Ecology

Habitat and Ecology
This species occupies a number of vegetation types and can be found in seasonal and nonseasonal forests, and in mangroves and swamps (Baumgarten and Williamson 2007). According to the last authors, A. palliata does not occur above 2,000 m, and most of its montane localities are at lower elevations.

The howler monkeys are the large leaf-eaters of the South American primate communities. Like the spider monkeys, they are prehensile-tailed, with a naked patch of skin on the under surface at the tip. Howler monkeys have small incisors and large, sexually dimorphic canines. The molar teeth are particularly adapted for their chewing leaves through shearing. 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). The red howlers (A. seniculus, A. macconnelli, A. juara, A. puruensis, and A. sara) have the largest voice boxes and the deepest roars, while the Mexican, Central American and northern Colombian mantled howlers, A. palliata and A. pigra, have the smallest, and their howls are more high pitched as a result.

The Mantled Howler Monkey is exceptional in the genus in that it may form large groups of more than 40 individuals, with a number of breeding males, although group size is generally less, averaging 14. For the other species, 14 is a large group, and they can usually be seen numbering four or five or up to 11 or so individuals. In the red howlers, there is usually only one dominant male in the group (occasionally two), others being sub-adults, or juveniles, along 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). The large groups of A. palliata may have home ranges extending to 60 ha (Estrada 1982), whereas in the llanos of northern Venezuela, home ranges of A. arctoidea can be as small as 4 ha (Sekulic 1982a).

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. Red howler monkeys have also been seen to eat and lick clay at so-called “salado” sites in the Colombian Amazon (Izawa 1975). The reason for this and the consumption of soil from termitaria is still not clearly understood, but may involve the need for certain minerals, or may be due to the properties of clay which, by adsorption, can reduce the effects of toxins ingested with leaves.

The diet of A. macconnelli has been studied by Mittermeier and van Roosmalen (1981) in Suriname and more recently during a long-term study in the Nouragues Field Station in French Guiana (Julliot and Sabatier 1993; Julliot 1994b,c, 1996a,b). It feeds mainly on soft parts of many different kinds of fruits, as well as flowers and young leaves. Also included in the diet are mature leaves, immature fruits, moss, bark, and the soil of termitaria. Julliot and Sabatier (1993) recorded the use of 195 plant species from 47 families. Seeds are ingested but only rarely eaten. As a result Alouatta, like Ateles, is an important seed disperser. Julliot (1996a) found that A. macconnelli dispersed the seeds of more than 95% of more than 100 plant species (especially Sapotaceae) from which they eat fruit over the two years of her observations.

Infant Alouatta are probably born throughout the year in Suriname, but data are not yet sufficient to determine if there is a birth peak. In Suriname, newborn infants have been seen in March, April, and November, and January (Mittermeier 1977). Crockett and Rudran (1987a,b) examined seasonal variation in births in red howlers from northern Venezuela, and found that they were less frequent during the early wet season (weaning would occur at the time of greatest food shortage). The llanos forests are more seasonal, however, than in the Guianas, and it is possible that this is not the case elsewhere. Oestrus lasts 2–4 days, with intervals between oestrous periods of about 17 days. Interbirth intervals are generally about 16.6 months, although they may be shortened by the death of an infant to about 10.5 months (Crockett and Sekulic 1984).

Size (see Glander (2006) for a discussion of body weight in mantled howling monkeys):
Adult male weight 7.15 kg (n=110+) (Peres 1994)
Adult female weight 5.35 kg (n=177+) (Peres 1994).

Costa Rica
Adult male weight 6.53 kg (n=14) (Glander et al. 1991)
Adult female weight 5.35 kg (n=18) (Glander et al. 1991).

Panama
Adult male weight 7.8 kg (n=15) (Thorington Jr. et al. 1979)
Adult female weight 6.6 kg (n=15) (Thorington Jr. et al. 1979)
See Glander (2006) for a discussion of body weight in mantled howling monkeys.

Systems
  • Terrestrial
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Mantled howler monkeys inhabit lowland and montane rain forests, including primary and regenerated forest habitats. Stoner (1996) researched two troops of mantled howler monkeys in northeastern Costa Rica to determine habitat selectivity within a lowland rainforest. She concluded that there was troop specific habitat selection occurring within the same area and significant intraspecific variability in foraging patterns. Following two study groups, she noted that one troop had a high utilization of primary forest (80%) over secondary forest, while the other preferred undisturbed riparian habitat (60%) to primary forest (30%).

Terrestrial Biomes: forest ; rainforest

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Found in lowland and montane rainforests including both primary and secondary forest (5) up to altitudes of 2000 m (3). They make use of all levels of the canopy, but it seems that the upper third is preferred (3).
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Trophic Strategy

Food Habits

Food resources consist mainly of leaves, fruit, and flowers, and vary seasonally with resource availability (Glander 1981). Flower availability is typically high during the dry season, and fruits are abundant during the wet season. Their diet is species-selective, and they graze almost exclusively on trees (Estrada and Coates-Estrada 1986). Food choice is influenced not only by digestibility and nutrient value, but also by secondary compounds (i.e. tannins) that may be undesirable (Glander 1981). While foraging, they spend nearly equal portions of their feeding time eating leaves as they do fruit, preferentially eating young leaves with higher protein to fiber ratio and lower tannin content (Estrada and Coates-Estrada 1986, Glander 1981). Sampling behavior may be important in adding new species to a social group's food base, and in testing seasonal changes in plant secondary compounds (Glander 1981).

This leaf grazing (folivorous) diet gives them access to a niche relatively unexploited by other mammals, so that they are often the most important arboreal mammalian folivore in a particular area. However, other competitors may impose significant pressure on available leaf resources, such as the leaf-cutting ant Atta cephalotus in Los Tuxtlas, Mexico. For a comprehensive list of plant species (34 species in 21 families) fed upon in a Mexican tropical rain forest setting, see Estrada and Coates-Estrada (1986). For a list of Costa Rican plant species, see Stoner (1996) and Glander (1981). Their feeding rate was calculated to be 53 g dry matter per kg each day (Nagy and Milton 1979). In other terms, an average sized individual would need to ingest 15% of its body size in fresh food per day during the dry season.

Plant Foods: leaves; fruit; flowers

Primary Diet: herbivore (Folivore )

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Life History and Behavior

Life Expectancy

Lifespan/Longevity

Average lifespan

Status: wild:
20.0 years.

Average lifespan

Status: wild:
25.0 years.

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Lifespan, longevity, and ageing

Maximum longevity: 24 years (captivity) Observations: In the wild, adults are estimated to live on average 16 years (Ronald Nowak 1999). One wild born female lived more than 15 years in captivity and could have been as old as 24 (Richard Weigl 2005).
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Reproduction

Mantled howler monkeys are polygynous.

Mating System: polygynous

Females reach sexual maturity at approximately 36 months, and are typically 42 months old by their first birth (Glander 1980). They undergo a regular estrus cycle, with an average duration of 16.3 days, and display sexual skin changes, particularly swelling and color change (from white to light pink) of the labia minora. Although the ovulation time is unknown, it may be predicted by the alpha male's behavior, as he copulates only at the midpoint of sexual skin swelling and remains uninterested at other times. Breeding occurs year-round, without any apparent seasonal variation, and a female generally participates in multiple matings before conception. The age of sexual maturity for males is 42 months, but males attempting to breed in non-maternal groups may be delayed until social status is gained, generally only if they are older than 6 years of age (Glander 1980). The typical copulatory sequence begins when a female approaches a male (typically within 1 meter) and begins rhythmic tongue movements while facing him (Young 1982). The male responds with rhythmic tongue movements, and within one minute the female turns and elevates her rump. Meanwhile the male has achieved an erection and immediately mounts the female, performs 5-20 pelvic thrusts over the duration of 20-60 seconds. The animals then turn sideways and disengage, and usually sit quietly for several minutes before slowly walking away (Young 1982). Pregnancy lasts an average of 186 days (6 months), and the interbirth interval is about 22.5 months (Glander 1980). Once the infant is 4 months old, it no longer has an influence on the mother's future reproduction, and if an infant dies within this 4-month period the interbirth interval shortens. The highest reproductive success occurs in the middle ranking females, with the alpha position lower possibly because of competitive pressures, and infant mortality appears to be lower when the timing of births in a group of females is clustered (Glander 1980).

Breeding interval: Females breed once every 22.5 months

Breeding season: Breeding occurs year-round

Average number of offspring: 1.

Average gestation period: 186 days.

Average age at sexual or reproductive maturity (female): 36 months.

Average age at sexual or reproductive maturity (male): 42 months.

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

Average birth mass: 409 g.

Average gestation period: 186 days.

Average number of offspring: 1.

Average age at sexual or reproductive maturity (male)

Sex: male:
1278 days.

Average age at sexual or reproductive maturity (female)

Sex: female:
1095 days.

Behavior of young mantled howler monkeys varies with age and size. Social exploration and play follows an inverted "U" pattern when plotted against increasing age, peaking at an early juvenile stage and decreasing with the increasing demand for energy in digestion and foraging (Baldwin and Baldwin 1978). Infants spend the first weeks of their life clinging to their mother and nursing, not mouthing leaves until 3 weeks of age and not leaving her side until the 5th week of life (Lyall 1996). In the 10th and 11th weeks, infants begin exploratory feeding and will spend a significant portion of their time independent of their mother.

Parental Investment: pre-fertilization (Provisioning, Protecting: Female); pre-hatching/birth (Provisioning: Female, Protecting: Female); pre-weaning/fledging (Provisioning: Female, Protecting: Female); pre-independence (Protecting: Female); extended period of juvenile learning

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Evolution and Systematics

Functional Adaptations

Functional adaptation

Sex of offspring controlled: mantled howler monkey
 

The reproductive tract of the female mantled howler monkey has electrical conditions that are altered to determine the sex of their offspring via medicinal plants.

   
  "Even more remarkable, studies in the 1990s by zoologist Dr. K. Glander of Duke University suggest that females of South America's mantled howler monkey (Alouatta palliata) may be actively employing pharmacological methods to determine the sex of their offspring. Glander noticed that the sex of a given female's offspring seemed to be directly related to the plants she had been eating at the time of mating. And the plants in turn controlled the electrical conditions present in the female's reproductive tract, either attracting or repelling those sperm carrying the male sex (Y) chromosome, which are believed to possess different electrical charges from those sperm carrying the female sex (X) chromosome." (Shuker 2001:215-216)
  Learn more about this functional adaptation.
  • Shuker, KPN. 2001. The Hidden Powers of Animals: Uncovering the Secrets of Nature. London: Marshall Editions Ltd. 240 p.
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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
Cuarón, A.D., Shedden, A., Rodríguez-Luna, E., de Grammont, P.C., Link, A., Palacios, E., Morales, A. & Cortés-Ortiz, L.

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

Contributor/s

Justification
This species is listed as Last Concern given its widespread distribution, presence in numerous protected areas, and because there are no major threats believed to be resulting in a significant range-wide population decline that would warrant listing in Near Threatened or a threatened category.

History
  • 2003
    Least Concern
    (IUCN 2003)
  • 2003
    Least Concern
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Current Listing Status Summary

Status: Endangered
Date Listed: 06/14/1976
Lead Region: Foreign (Region 10) 
Where Listed: Entire


Population detail:

Population location: Entire
Listing status: E

For most current information and documents related to the conservation status and management of Alouatta palliata , see its USFWS Species Profile

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The mantled howler monkey is classified as endangered in the United States Endangered Species Act of 1991 and vulnerable in CITES Appendix I. Under pressure from rainforest fragmentation, many howlers have moved into shaded cacao and coffee plantations where forest habitat has disappeared, especially in southern Mexico (Estrada et al. 1999). Continual decline may have severe implications for rainforest habitats, as howler monkeys play an important role in seed dispersal, and their fresh dung constitutes an important resource for dung beetles. Dung beetles use the howler excrement for both food and oviposition sites, and so dung beetle abundance is closely correlated with howler monkey abundance. It has been suggested that dung beetles are good biodiversity indicators, but they are also intrinsically important in their role as secondary seed dispersers and nutrient cyclers. A population analysis conducted by Cortes-Ortiz et al. (1996) in southern Mexico estimated that a total of 1,352 individual mantled howler monkeys inhabit protected areas, while 10,249 remain in unprotected habitat. Possible threats include habitat fragmentation and natural disasters. Cortes-Ortiz et al. (1996) suggest better managing of protected areas, establishing new reserves, developing translocation programs, managing populations within fragmented areas, controlling human traffic, promoting education and collaborating with other institutions.

Some evidence suggests that mantled howler monkey populations are becoming robust once again. The population on Barro Colorado Island is one example, where it suffered a severe decline resulting from a yellow fever epidemic (Collias and Southwick 1951), but returned to a robust size by the late 1970's (Nagy and Milton 1979). Also, evidence from La Pacifica, Costa Rica indicates that regenerating forest is becoming habitable to mantled howler monkeys, where dispersal and the formation of new social groups has been occurring (Glander 1992).

US Federal List: endangered

CITES: appendix i

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 under Appendix I of CITES (4). There are five subspecies: the Mexican howler monkey (A. p. mexicana) and the Azuero howler monkey (A. p. trabeata) are classified as Critically Endangered (CR), the Ecuadorian mantled howler monkey (A. p. aequatorialis) and the Coiba Island howler monkey (A. p. coibensis) are classified as Vulnerable (VU), and the golden mantled howler monkey (A. p. palliata) is classified as Least Concern (LC) on the IUCN Red List (1).
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Population

Population
Alouatta palliata palliata
This subspecies is known to occur in densities of 8–10 individuals/ha in fragmented habitats. In Nicaragua (Williams-Guillen, Otterstrom, Hagell, Gomez-Fuentes, 2007) and Costa Rica this subspecies is abundant.

Alouatta palliata mexicana
Although this subspecies has a very restricted range, encompassing areas of highly disturbed vegetation with extremely high rate of loss, in some fragments the subspecies may be locally common.

Alouatta palliata aequatorialis
In one study in Colombia, 20 individuals/km² were recorded near a biological station Armargal (Ramirez-Sanchez 2003). Recent faunal surveys in Utria National Park found them to be extremely rare, in areas where they were much more common in years past (H. Rubio pers. comm.). On the Osa pennisula, Costa Rica, in Corcovado National Park, densities were recorded at 0.2 groups/km² and in Golfo Dulce at 0.1/groups/km² (Carrillo et al. 2000).

Alouatta palliata trabeata
There is an observation of 430 individuals in 35 troops recorded within 355 km² of fragmented forest (Méndez-Carvajal 2005).

Population Trend
Unknown
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Threats

Major Threats
Across its range, there are no major threats, although it is certainly susceptible to hunting and habitat loss. For example, forests on the Azuero Peninsula (the range of A. p. trabeata) have been largely destroyed and are highly fragmented. Likewise, habitat within the range of A. p. mexicana are known to have experienced very high rates of decline (Cuarón 1997).

In the Chocó region of Colombia, Alouatta palliata aequatorialis is at risk of widespread hunting by Afro-Colombian and indigenous people. Furthermore, over 90% of forests on the Atlantic coast of Colombia have been destroyed for agricultural and pasture; it is estimated that at least 31% of forest has been lost over the past 10 years alone (based on calculations from satellite photos; Miller et al. 2004). Ground truthing of this data found only 2.5% of viable secondary forest habitat remaining in this region (Miller et al. 2004).
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Throughout its range, this howler monkey is threatened by forest destruction and fragmentation (5). In areas where forest destruction has been particularly severe, the species often moves into cocoa and coffee plantations (5). Mantled howler monkeys play a key role in the regeneration and health of its rainforest habitats, as they disperse seeds in their dung. Furthermore, their dung is an important resource for a diverse range of dung beetles, which are responsible for the recycling of nutrients from the dung back into the soil (5). The Critically Endangered Mexican subspecies (Alouatta palliata mexicana) has suffered greatly from fragmentation of its habitat. An estimated future decline of 73 - 84% over 30 years has been projected, and habitat loss is ongoing (1). Small, highly isolated populations are unable to disperse naturally; they are at inherent risk of local extinction caused by chance events, such as natural disasters or outbreaks of disease, as well as genetic problems as a result of inbreeding.
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Management

Conservation Actions

Conservation Actions
This species occurs, or may occur, in several protected areas:

Alouatta palliata palliata
Costa Rica
Santa Rosa National Park (21,913 ha) (Fedigan and Rose 1995; Matamoros et al. 1996; Matamoros and Seal 2001)
Rincón La Vieja National Park (14,083 ha) (Matamoros et al. 1996)
Palo Verde National Park (5,704 ha) (Matamoros et al. 1996)
Tortuguero National Park (18,946 ha) (in range)
Braulio Carrillo National Park (44,898 ha) (Matamoros et al. 1996; Matamoros and Seal 2001)
Manuel Antonio National Park (682 ha) (Matamoros et al. 1996)
Volcán Irazú National Park (2,309 ha) (in range)
Cahuita National Park (1,067 ha) (in range)
La Amistad (Talamanca) International Park (193,929 ha) (in range)
Chirripó National Park (50,150 ha) (in range)
Corcovado National Park (41,788 ha) (Matamoros et al. 1996)
Guanacaste National Park (33,786 ha) (Matamoros et al. 1996)
Volcán Tenorio National Park (12,819 ha)
Piedras Blancas National Park (14,100 ha)
Lomas de Barbudal Biological Reserve (2,279 ha) (Chapman et al. 1989)
Carara Biological Reserve (4,700 ha) (Matamoros et al. 1996)
Hitoy Cerere Biological Reserve (9,154 ha) (Matamoros et al. 1996)
Alberto Manuel Brenes Biological Reserve (7,683 ha) (in range)
Cabo Blanco Strict Nature Reserve (14,258 ha) (Lippold 1989)
La Selva Protection Zone (2,815 ha) (Fishkind and Sussman 1987; Campbell and Sussman 1994)

Honduras
Punta Sal National Park (78,200 ha) (Matomoros and Seal 2001)
Montaña de Cusuco National Park (18,000 ha) (Marineros and Gallegos 1998)
Pico Bonito National Park (68,000 ha) (Marineros and Gallegos 1998; Matomoros and Seal 2001)
Pico Pijol National Park (11,400 ha) (in range)
Montaña de Yoro National Park (15,500 ha (Marineros and Gallegos 1998)
Santa Bárbara National Park (13,000 ha) (Matomoros and Seal 2001)
Cerro Azul Meambar National Park (39,000 ha (Marineros and Gallegos 1998)
Sierra de Agalta National Park(27,000 ha) (Marineros and Gallegos 1998)
Celaque National Park(18,000 ha (in range)
Montaña de Comayagua National Park (9918,000 ha) (in range)
Montecristo-Trifinio National Park (5,400 ha) (in range
La Tigra National Park (7,571 ha) in range)
Laguna de Guaymoreto (5,000 ha) ((Marineros and Gallegos 1998)
Capiro Calentura National Park (5,500 ha) (Matomoros and Seal 2001)
Laguna de Caratasca Wildlife Refuge (120,000 ha) (in range)
Misoco Biological Reserve (4,600 ha) (in range)
Volcán Pacayita Biological Reserve (9,700 ha) (in range)
Guisayote Biological Reserve (7,000 ha) (in range)
El Pital Biological Reserve (3,800 ha) (in range)
Opalaca Biological Reserve (14,500 ha) (in range)
El Chile Biological Reserve (6,000 ha (in range)
Montecillos Biological Reserve (12,500 ha) (in range)
Montaña San Pablo Biological Reserve (in range)
Guajiquiro Biological Reserve (7,000 ha) (in range
Yerba Buena Biological Reserve (3,600 ha) (in range)
Chiflador Biological Reserve (500 ha) (in range
Uyuca Biological Reserve (1,100 ha) (in range
Yuscarán Biological Reserve (2,300 ha) (in range)
Río Negro Biological Reserve (60,000 ha) (in range)
Barras Cuero y Salado Wildlife Refuge (12,300 ha) (Marineros and Gallegos 1998; Matamoros and Seal 2001)
Texiguat Wildlife Refuge (10,000 ha) (in range)
La Muralla National Park 7,000 ha (Marineros and Gallegos 1998; Matamoros and Seal 2001)
El Armado Wildlife Refuge (3,500 ha) (in range)
Erapuca Wildlife Refuge (5,600 ha) (in range)
Puca Wildlife Refuge (4,900 ha) (in range
Montaña Verde Wildlife Refuge (8,300 ha) (in range)
Mixcure Wildlife Refuge (8,000 ha) (in range
Montaña de Corralitos (5,500 ha) (in range)

Nicaragua
Saslaya National Park (11,800 ha) (in range)
Volcán Masaya National Park (5,500 ha) (in range)
Archipelago Zapatera (5,227 ha) (in range)
Rio Escalante – Chococente Wildlife Refuge (4,800 ha) (in range)
Bismuna – Pahau – Cayos – Miskitos (80,000 ha) (in range)
Cerros de Bana Cruz Natural Reserve (10,100 ha) (in range)
Cordiella Diplito y Jalapa (1,500 ha) (in range)
Laguna Wonta (30,000 ha) (in range)
Cerro Wailwas (1,200 ha) (in range)
Kilambe Natural Reserve (6,000 ha (in range)
Peñas Blancas (7,000 ha) (in range)
Santa Maria de Osuma (2,000 ha) (in range)
Lagunas de Wancarlaya (8,000 ha) (in range)
Salto del Rio Estanzuela (200 ha) (in range)
Cerro Musún Natural Reserve (4,100 ha) (in range)
Boca del Rio Grande de Matagalpa (68,000 ha) (in range)
Lagunas Tecomapa, Moyua y La Playitas (in range)
Cordillera de Amerisque Natural Reserve (1,500 ha (in range)
Costa Sur del Pacifico (2,000 ha) (in range)
Cerro Tomasu (2,000 ha) (in range)
Volcán Cosiguina Natural Reserve (12,240 ha (in range)
Estero Real Natural Reserve (38,725 ha) (in range)
Complejo Volcánico Momotombo y Momotombito Natural Reserve (10,000 ha) (in range)
Peninsula de Chiltepe (1,800 ha) (in range)
Laguna de Tisma Natural Reserve (4,438 ha) (in range)
Volcán Mombacho – Laguna Mecatepe Natural Reserve (2,847 ha) (reported) (Crockett et al. 1997)
Volcan Madera Natural Reserve (4,100 ha) (in range)
Volcán Concepción Natural Reserve (2,200 ha) (in range)
Los Maribios (in range)
Estero Padre Ramos Natural Reserve (7,815 ha) (in range)
Reserva de la Biosfera Bosawas (1,100,000 ha) (Crockett et al. 1997)
Refugio Bartola / Río Indio-Maíz Biological Reserve (295,000 ha) (Crockett et al. 1997)

Alouatta palliata mexicana
Guatemala
Rio Dulce National Park (24,200 ha) (Curdts 1993; Silva-López et al. 1995, 1998)
Colcán Pacaya National Park (4,800 ha) (in range)
Lake Atitlan National Park (3,250 ha) (possible, Matamoros and Seal 2001)
Sipacate-Naranjo National Park (2,000 ha) (in range)
Biotopo Mario Dary Rivera Quetzal (1,150 ha) (A. pigra according to Curdts (1993), but A. palliata according to Silva-López et al. 1995, 1998; Matamoros and Seal 2001)
Biotopo de Chocon Machacas (7,000 ha) (sympatric with A. pigra; Curdts 1993; Silva-López et al. 1995, 1998; Matamoros and Seal 2001)
Biotopo Cerro Cahui (700 ha) (Silva-López et al. 1998; Matamoros and Seal 2001)
Biotopo San Miguel La Palotada (49,300 ha) (sympatric with A. pigra; Curdts 1993; Silva-López et al. 1995, 1998; Matamoros and Seal 2001)
Sierra de las Minas Biosphere Reserve (236,300 ha) (Silva-Lopes et al. 1995) (Sympatric with A. pigra; Curdts 1993; Silva-López et al. 1995, 1998; Matamoros and Seal 2001)

Mexico
Cañon del Sumidero National Park (21,789 ha) (Estrada and Coates-Estrada 1984)
Volcán de San Martin Special Biosphere Reserve (1,500 ha) (Estrada and Coates-Estrada 1988; Mexico, SEDUE, 1989; Matamoros and Seal 2001)
Sierra de Santa Marta Special Biosphere Reserve (20,000 ha) (Silva-López 1982; Silva-López and Portilla-Ochoa 2002; Silva-López and Garcia-Orduña 1984; Silva-López et al. 1988, 1993; Matamoros and Seal 2001).
Selva del Ocote Special Biosphere Reserve (48,140 ha) ( Matamoros and Seal 2001)
El Triunfo National Biosphere Reserve (119,595 ha) (in range)
Estación Biologica Tropical ‘Los Tuxtlas” (700 ha) (Estrada and Coates-Estrada 1994)
Naja (Hernandez-Yañez pers. comm. in Rodríguez-Luna et al. 1996)
Metzaboc (Hernandez-Yañez pers. comm. in Rodríguez-Luna et al. 1996)
Parque La Venta Municipal Park (8 ha) (Fuentes et al. 2003)
Parque Yumká Municipal Park (101 ha) (Estrada et al. 2001; Del Valle et al. 2001; Muñoz et al. 2002)

Alouatta palliata aequatorialis
Colombia
Ensenada de Utría Natural National Park (54,300 ha) (Defler 1994)
Los Katios Natural National Park (72,000 ha) (Defler 1994)
Munchique Natural National Park (44,000 ha) (possibly, Defler 1994)
Sanquinaga Natural National Park (80,000 ha) (Defler 1994)
Paramillo Natural National Park (460,000 ha) (possibly, Defler 1994)
Los Farallones Natural National Park (150,000 ha) (possibly, Defler 1994)

Ecuador
Machalilla Nartional Park (56,814 ha) (Tirira 2007)
Cotacachi-Cayapas Ecological Reserve (243,638 ha) (Tirira 2007)
Mache-Chindul Ecological Reserve (119,172 ha) (Tirira 2007)
Manglares Churute Ecological Reserve (49,894 ha) (Tirira 2007)
Los Cedros Protected Forest (Tirira 2007)

Panama
Porto Belo National Park (34,848 ha) (in range)
Chagres National Park (129,000 ha) (in range)
La Amistad International Park (207,000 ha) (in range)
Soberanía National Park (22,104 ha) (in range)
El Copé – Comar Torrijos Herrera (25,275 ha) (in range)
Volcán Baru National Park (14,000 ha) (in range)
Altos de Campana National Park (4,816 ha) (in range)
Darién National Park (555,000 ha) (in range)
La Fortuna Water Production Reserve (26,000 ha) (in range)
La Yeguada Forest Reserve (7,090 ha) (in range)
Canglón National Park (31,650 ha) (in range)
Cienega de Changuinola (in range)
Peninsula Valiente (in range)
Estero Rio Bayano (in range)
Cienega de Urey (in range)
Ensenada de Copal (in range)
Estero Golfo de San Miguel (in range)
Cienega de Matsugarati (in range)
Cerre Cerrezuela – Rio Grande (in range)
Estero Bahia de Muertos (in range)
Playa de la Barqueta Agricola (5,935 ha) (in range)
Estero Río Fonseca (in range)
Estero Ríos Tabasara – Bubi (in range)
Estero Golfo de Montijo Recreation Area (89,452 ha) (in range)
Palo Seco Protection Forest (244,000 ha) (in range)
Serranias de Majé (in range)
Cayo Swan (in range)
Cayo Tigre (in range)
Lagunas del Volcán (142 ha) (in range)
Cerro Gaital (in range)
Cerro Chame (in range)
Picachos de Ola (in range)
Gran Valera de Chorcha (in range)
Isla Barro Colorado Natural Monument (5,600 ha) (Carpenter 1965)
Isla de Majé Scientific Reserve (1,433 ha) (in range)
Kunayala Private Reserve (2,357 ha) (in range)
Golfo de Chiriquí National Park (14,740 ha) (in range)
Lago Gatún Recreation Area (348 ha) (in range)
Metropolitano Natural Park (265 ha) (in range)
Alto de Darien Protection Forest (201,000 ha) (in range)
San San Pond Sak (16,125 ha) (in range)
Punta Patiño (13,805 ha) (in range)
Los Pozos de Calobre(3.5 ha) (in range)
El Salto de Las Palmas (348 ha) (in range)
Camiño de Cruces National Park (4,000 ha) (in range)
Filo del Tallo (in range)
Maski Private Reserve (544 ha) (in range)
San Blas Reserve (141,000 ha) (in range)

Alouatta palliata coibensis
Panama
Isla Coiba National Park and Jicarón (270,125 ha) (Milton and Mittermeier 1977)

Alouatta palliata trabeata
Panama
Cerro Hoya National Park (32,557 ha) (Rowe 2000; Matamoros and Seal 2001).

It is listed on Appendix I of CITES.
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Conservation

The mantled howler monkey is protected from international trade by its listing under Appendix I of the Convention on International Trade in Endangered Species (CITES) (4). It has been estimated that around 1,352 individuals are located within protected areas; however, a further 10,249 occur on unprotected land (5). It has been proposed that new reserves should be established to protect the species, and that translocation programmes should be set up to combat the effects of isolation. In parallel to these measures, it is essential that local environmental education programmes about the importance of the species and its imperilled status should be initiated (5).
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Relevance to Humans and Ecosystems

Benefits

Economic Importance for Humans: Positive

A small number of mantled howler monkeys are utilized for scientific experimentation.

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Wikipedia

Mantled howler

The mantled howler (Alouatta palliata), or golden-mantled howling monkey, is a species of howler monkey, a type of New World monkey, from Central and South America. It is one of the monkey species most often seen and heard in the wild in Central America. It takes its "mantled" name from the long guard hairs on its sides.

The mantled howler is one of the largest Central American monkeys, and males can weigh up to 9.8 kg (22 lb). It is the only Central American monkey that eats large quantities of leaves; it has several adaptations to this folivorous diet. Since leaves are difficult to digest and provide less energy than most foods, the mantled howler spends the majority of each day resting and sleeping. The male mantled howler has an enlarged hyoid bone, a hollow bone near the vocal cords, which amplifies the calls made by the male, and is the reason for the name "howler". Howling allows the monkeys to locate each other without expending energy on moving or risking physical confrontation.

The mantled howler lives in groups that can have over 40 members, although groups are usually smaller. Most mantled howlers of both sexes are evicted from the group they were born in upon reaching sexual maturity, resulting in most adult group members being unrelated. The most dominant male, the alpha male, gets preference for food and resting places, and mates with most of the receptive females. The mantled howler is important to the rainforest ecology as a seed disperser and germinator. Although it is impacted by deforestation, it is able to adapt better than other species, due to its ability to feed on abundant leaves and its ability to live in a limited amount of space.

Taxonomy[edit]

The mantled howler belongs to the New World monkey family Atelidae, the family that contains the howler monkeys, spider monkeys, woolly monkeys and muriquis. It is a member of the subfamily Alouattinae and genus Alouatta, the subfamily and genus containing all the howler monkeys.[1][3] The species name is A. palliata; a pallium was a cloak or mantle worn by ancient Greeks and Romans.[4] This refers to the long guard hairs, known as a "mantle", on its sides.[5]

Three subspecies are recognized:[3]

Two additional subspecies of the mantled howler are sometimes recognised, but these are more generally recognised as subspecies of the Coiba Island howler, Allouatta coibensis. However, mitochondrial DNA testing of their status has been inconclusive:[3]

Physical description[edit]

Mantled howlers resting

The mantled howler's appearance is similar to other howler monkeys of the genus Alouatta except for coloration. The mantled howler is primarily black except for a fringe of yellow or golden brown guard hairs on the flanks of the body earning the common name "mantled" howler monkey.[6] When the males reach maturity, the scrotum turns white.[7] Females are between 481 and 632 mm (18.9 and 24.9 in) in body length, excluding tail, and males are between 508 and 675 mm (20.0 and 26.6 in). The prehensile tail is between 545 and 655 mm (21.5 and 25.8 in) long. Adult females generally weigh between 3.1 and 7.6 kg (6.8 and 16.8 lb), while males typically weigh between 4.5 and 9.8 kg (9.9 and 21.6 lb).[7] Average body weights can vary significantly between monkey populations in different locations.[8] The brain of an adult mantled howler is about 55.1 g (1.94 oz), which is smaller than that of several smaller monkey species, such as the white-headed capuchin.[7][9]

The mantled howler shares several adaptations with other species of howler monkey that allow it to pursue a folivorous diet, that is, a diet with a large component of leaves. Its molars have high shearing crests, to help it eat the leaves,[10] and males have an enlarged hyoid bone near the vocal cords.[11] This hyoid bone amplifies the male mantled howler's calls, allowing it to locate other males without expending much energy.[11]

Behavior[edit]

Social structure[edit]

The mantled howler lives in groups. Group size usually ranges from 10 to 20 members, generally 1 to 3 adult males and 5 to 10 adult females, but some groups have over 40 members.[10][12] Males outrank females, and younger animals of each gender generally have a higher rank than older animals.[11] Higher-ranking animals get preference for food and resting sites, and the alpha male gets primary mating rights.[11] Animals in the group are generally not related to each other because most members of both sexes leave the group before sexual maturity.[10]

Grooming activity in the mantled howler is infrequent and has been shown to reflect social hierarchy, with dominant individuals grooming subordinates.[13][14] Most grooming activities are short and are typically females grooming infants or adult males.[15] Aggressive interactions between group members is not often observed either.[13] However, studies have shown that aggressive interactions among group members do occur, and are probably not often observed because these interactions tend to be quick and silent.[13]

Mantled howler groups that have been studied have occupied home ranges of between 10 and 60 hectares (25 and 148 acres).[10] Groups do not defend exclusive territories, but rather several groups have overlapping home ranges.[11] However, if two groups meet each group will aggressively attempt to evict the other.[11] On average, groups travel up to about 750 metres (2,460 ft) each day.[10]

The mantled howler has little interaction with other sympatric monkey species but interactions with the white-headed capuchin sometimes occur. These are most often aggressive, and the smaller capuchins are more often the aggressors.[16] However, affiliative associations between the capuchins and howlers do sometimes occur, mostly involving juveniles playing together, and at times the capuchins and howlers may feed in the same tree, apparently ignoring each other.[16]

Diet[edit]

The mantled howler is the most folivorous species of Central American monkey. Leaves make up between almost 50% and 75% of the mantled howler's diet.[10][12] The mantled howler is selective about the trees it eats from, and it prefers young leaves to mature leaves.[17] This selectivity is likely to reduce the levels of toxins ingested, since certain leaves of various species contain toxins.[17] Young leaves generally have less toxins as well as more nutrients than more mature leaves, and are also usually easier to digest.[10][17] Mantled howler monkeys possess large salivary glands that help break down the leaf tannins by binding the polymers before the food bolus reaches the gut.[15] Although leaves are abundant, they are a low energy food source.[11] The fact that the mantled howler relies so heavily on a low energy food source drives much of its behaviour – for example, howling to locate other groups and spending a large portion of the day resting.[11]

Although leaves tend to make up the majority of the mantled howler's diet, fruit can also make up a large portion of the diet. When available, the proportion of fruit in the diet can be as much as 50%, and can sometimes exceed the proportion of leaves.[10] The leaves and fruit from Ficus trees tend to be the preferred source of the mantled howler.[11] Flowers can also make up a significant portion of the diet and are eaten in particularly significant quantities during the dry season.[10][11] The mantled howler tends to get the water it needs from its food, drinking from tree holes during the wet season,[11] and by drinking water trapped in bromeliads.[18]

Like other species of howler monkeys, almost all mantled howlers have full three color vision.[19][20] This is different from other types of New World monkeys, in which most individuals have two color vision. The three color vision exhibited by the mantled howler is believed to be related to its dietary preferences, allowing it to distinguish young leaves, which tend to be more reddish, from more mature leaves.[19]

Locomotion[edit]

Mature male showing prehensile tail and white scrotum

The mantled howler is diurnal and arboreal.[7] Movement within the rainforest canopy and floor includes quadrupedalism (walking and running on supports), bridging (crossing gaps by stretching), and climbing.[21] It will also sometimes leap to get to another limb.[22]

However, the mantled howler is a relatively inactive monkey. It sleeps or rests the entire night and about three quarters of the day. Most of the active period is spent feeding, with only about 4% of the day spent on social interaction.[22] This lethargy is an adaptation to its low energy diet.[11] It uses its prehensile tail to grasp a branch when sleeping, resting or when feeding.[23] It can support its entire body weight with the tail, but more often holds on by the tail and both feet.[23] A study has shown that the mantled howler reuses travel routes to known feeding and resting sites, and appears to remember and use particular landmarks to help pick direct routes to its destination.[24]

Communication[edit]

The mantled howler gets the name "howler" from the calls made by the males, particularly at dawn and dusk, but also in response to disturbances.[11] These calls are very loud and can be heard for several kilometers.[11] The calls consist of grunts and repeated roars that can last for four to five seconds each.[11] The volume is produced by the hyoid bone — a hollow bone near the vocal cords — amplifying the sound made by the vocal cords. Male mantled howlers have hyoid bones that are 25 times larger than similarly sized spider monkeys, and this allows the bone to act like the body of a drum in amplifying the calls. Females also call but their calls are higher in pitch and not as loud as the males'.[11] The ability to produce these loud roars is likely an energy saving device, consistent with the mantled howler's low energy diet. The roars allow the monkey to locate each other without moving around or risking physical confrontations.[11] The mantled howler uses a wide range of other sounds, including barks, grunts, woofs, cackles and screeches.[18] It uses clucking sounds to maintain auditory contact with other members of its group.[25]

Male mantled howler howling in the trees

The mantled howler also uses non-vocal communication, such as "urine rubbing" when in a distressful social situation.[18] This consists of rubbing the hands, feet, tail and/or chest with urine.[18] It marks its scent by rubbing its throat on branches.[7] Lip smacking and tongue movements are signals used by females to indicate an invitation to mate.[18] Genital displays are used to indicate emotional states, and group members shake branches, which is apparently a playful activity.[18]

The mantled howler is usually indifferent to the presence of humans. However, when it is disturbed by people, it often express its irritation by urinating or defecating on them. It can accurately hit its observers despite being high in the trees.[11]

Tool use[edit]

The mantled howler has not been observed using tools, and prior to 1997 no howler monkey was known to use tools. However, in 1997 a Venezuelan red howler (Alouatta seniculus) was reported to use a stick as a club to hit a Linnaeus's two-toed sloth, (Choloepus didactylus), that was resting in its tree.[26] This suggests that other howlers, such as the mantled howler, may also use tools in ways that have not yet been observed.

Reproduction[edit]

Juvenile in a Costa Rican Pacific dry forest

The mantled howler uses a polygamous mating system in which one male mates with multiple females.[18] Usually, the alpha male monopolises the breeding opportunities, but if the alpha male is distracted, a lower-ranking male can get an opportunity to mate.[11] And in some groups, lower-ranking males do get regular mating opportunities and do sire offspring.[10][27] Alpha males generally maintain their status for about 2½ to 3 years, during which time they may father 18 or so infants.[7] Females become sexually mature at 36 months, males at 42 months.[18] Females reaching sexual maturity are typically 42 months old by their first birth. They undergo a regular estrus cycle, with an average duration of 16.3 days, and display sexual skin changes, particularly swelling and color change (from white to light pink) of the labia minora.[28] The copulatory sequence begins when a receptive female approaches a male and engages in rhythmic tongue flicking. The male responds with the same tongue movements before the female turns while elevating her rump, which allows for mating to begin.[11][18][29] Females apparently also use chemical signals, since males smell the females' genitals and taste their urine.[18] The gestational period is 186 days; births can occur at any time of year.[18] The infant's fur is silver at birth, but turns pale or gold after a few days. After that, the fur starts to darken, and the infant takes on the adult coloration at about 3 months old.[11]

The infant is carried under its mother, clinging to its mother's chest, for the first 2 or 3 weeks of its life.[18] After that, it is carried on its mother's back.[18] At about 3 months the mother will usually start to push the infant off, but will still carry the infant some of the time until it is 4 or 5 months old.[11] After the young can move on its own, the mother will carry it across difficult gaps in the trees.[18] Juveniles play among themselves much of the time.[18] Infants are weaned at 1½ years old at which point maternal care ends.[18] Adult females typically give birth every 19 to 23 months, assuming the prior infant survived to weaning.[10]

The mantled howler differs from other howler monkey species in that the males' testes do not descend until they reach sexual maturity.[15] Upon reaching sexual maturity, the young monkeys are usually evicted from their natal group, although the offspring of a high-ranking female may get to stay in its natal group.[11] However, many infants do not reach sexual maturity; high-ranking adults sometimes harass or kill the offspring of lower-ranking monkeys to eliminate competition to their own offspring for an opportunity to remain with the group upon reaching maturity.[11] Natal emigration is performed by both sexes, with 79% of all males and 96% of the females leaving their original social group.[30] When a male from outside the group ousts the previous alpha male, he normally kills any infants so that the mothers come into estrus quickly and are able to mate with him.[10] Predators such as cats, weasels, snakes and eagles also kill infants.[11] As a result, only about 30% of mantled howler infants live more than one year.[5] The highest reproductive success occurs in the middle-ranking females, with the alpha position lower possibly because of competitive pressures, and infant mortality appears to be lower when the timing of births in a group of females is clustered.[28] If it survives infancy, the mantled howler's lifespan is typically 25 years.[5]

Distribution and habitat[edit]

Mantled howler in a wildlife sanctuary, Gulf of Dulce, Costa Rica

The mantled howler is native to Colombia, Costa Rica, Ecuador, Guatemala, Honduras, Mexico, Nicaragua, Panama and Peru.[3] Within Honduras, Nicaragua, Costa Rica and Panama, the mantled howler is found in locations throughout the countries.[3] In Colombia and Ecuador, it is found in a narrow corridor bordered by the Pacific Ocean to the west and the Andes Mountains to the east and also in Colombia in a small area near the Caribbean Sea close to the Panama border.[3] In Guatemala, the mantled howler is found through the central part of the country, and into southeastern Mexico south of the Yucatán Peninsula.[3] The mantled howler is among the most commonly seen and heard primates in many Central American national parks, including Manuel Antonio, Corcovado, Monteverde and Soberania.[12][31] The mantled howler lives in several different types of forest, including secondary forest and semi-deciduous forest but is found in higher densities in older areas of forest and in areas containing evergreen forest.[32][33] The mantled howler is sympatric with another howler monkey species, the Guatemalan black howler, A. pigra, over a small part of its range, in Guatemala and Mexico near the Yucatan Peninsula.[3]

Conservation status[edit]

The mantled howler is regarded as "least concern" from a conservation standpoint by the IUCN. Nonetheless, its numbers may be adversely impacted by rainforest fragmentation which has caused forced relocation of groups to less habitable regions. However, the mantled howler can adapt to forest fragmentation better than other species due to its low energy lifestyle, small home ranges and ability to exploit widely available food sources.[34] The mantled howler is important to its ecosystems for a number of reasons, but especially in its capacity as a seed disperser and germinator, since passing through the monkey's digestive tract appears to aid the germination of certain seeds.[11] Dung beetles, which are also seed dispersers as well as nutrient recyclers, also appear to be dependent on the presence of the mantled howler.[11] The mantled howler is protected from international trade under Appendix I of the Convention on International Trade in Endangered Species (CITES).[35]

References[edit]

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  23. ^ a b Kavanagh, M. (1983). A Complete Guide to Monkeys, Apes and Other Primates. London: Cape. pp. 95–98. ISBN 0-224-02168-0. 
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  25. ^ da Cunha, R.G.T. and Byrne, R. (2009). "The Use of Vocal Communication in Keeping the Spatial Cohesion of Groups: Intentionality and Specific Functions". In Garber, P., Estrada, A. Bicca-Marques, J.C., Heymann, E. and Strier, K. South American Primates: Comparative Perspectives in the Study of Behavior, Ecology and Conservation. Springer. pp. 344–345. ISBN 978-0-387-78704-6. 
  26. ^ Richard-Hansen, C., Bello, N., & Vie, J. (1998). "Tool use by a red howler monkey (Alouatta seniculus) towards a two-toed sloth (Choloepus didactylus)". Primates 39 (4): 545–548. doi:10.1007/BF02557575. 
  27. ^ Di Fiore, A. (2009). "Genetic Approaches to the Study of Dispersal and Kinship in New World Primates". In Garber, P., Estrada, A., Bicca-Marques, J.C., Heymann, E. and Strier, K. South American Primates: Comparative Perspectives in the Study of Behavior, Ecology and Conservation. Springer. pp. 223–225. ISBN 978-0-387-78704-6. 
  28. ^ a b Glander, Ken (1980). "Reproduction and Population Growth in Free-Ranging Mantled Howler Monkeys". American Journal of Physical Anthropology 53 (53): 25–36. doi:10.1002/ajpa.1330530106. PMID 7416246. 
  29. ^ Young, O (1982). "Tree-rubbing Behavior of a Solitary Male Howler Monkey". Primates 2 (23): 303–306. doi:10.1007/BF02381169. 
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