Alouatta caraya
Creators: name: Russell A. Mittermeier
name: Anthony B. Rylands
name: Don E. Wilson
Publisher: name: Lynx Edicions
Year: 2013
Subjects: Biodiversity
Taxonomy
Animalia
Chordata
Mammalia
Primates
Atelidae
Alouatta
Alouatta caraya

description: 10.
Paraguayan Howler
Alouatta caraya
French: Hurleur noir / German: Schwarzer Brullaffe / Spanish: Mono aullador caraya Other common names: Black Howler/Howling Monkey, Black-and-gold Howler
Taxonomy. Simia caraya Humboldt, 1812,
Paraguay.
Molecular genetic studies have shown that this species is sister to the Amazonian red howlers (A. seniculus, A. sara, and A. macconnelli); they diverged from a common ancestor c.4 million years ago. A. caraya hybridizes with A. guariba in certain narrow zones of contact in northern Argentina (Misiones Province) and southern Brazil (states of Parana and Rio Grande do Sul). Monotypic.
Distribution. C Brazil (S of the states of Para, Tocantins, Maranhao —upper Rio Paranaiba—and Piaui, also in W Bahia, Rondonia, Mato Grosso —N to Rio Arrais, W to the Pantanal in the Rio Paraguay Basin, Goias, Minas Gerais, and Mato Grosso do Sul states; in the S, it occupies the bush savanna (cerrado) regions of the Rio Parana Basin in the N and NW of Sao Paulo State, and the W ofthe states of Parana, Santa Catarina, and Rio Grande do Sul), N Argentina (Misiones, Corrientes, E of Formosa and Chaco, and N of Santa Fe provinces, in the basins of the rios Parana, Uruguay, and Paraguay), Paraguay (E forests and in some areas of the Chaco where it occupies gallery forests along the rios Paraguay and Pilcomayo), and E & SE Bolivia (as far S as the Yungas of Chuquisaca and Tarija departments and the headwaters of the rios Pilcomayo and Pilaya); its distribution may also extend into the NW of Uruguay.
Descriptive notes. Head—-body 60-65 cm (males) and ¢.50 cm (females), tail 60-65 cm (males) and 54-5-60 cm (females); weight 5-3-9-6 kg (males) and 3-6-6-5 kg (females). Adult Paraguayan Howlers are sexually dichromatic, but both sexes are born blonde with hair that gradually changes to adult colors. As adults, mature males are generally uniformly black, and females and young of either sex are pale grayish-yellow or golden-brown. Male Paraguayan Howlers from Bahia and Goias are black, while those from Mato Grosso and Parana have a brown back and hind parts, in addition to a black head and forequarters. Males from Sao Paulo and Minas Gerais, meanwhile, are brown-black with yellowish hands, feet, belly, and tail tip. Underparts of adult females are sometimes tinged with orange, and there is a darker brown to grayish line that runs from the crown along the back to the base of the tail. In all individuals, the face is invariably dark,fur is stiff and lengthy, and the beard is prominent. Hairs on the crown grow entirely forward from a whorl on the nape to overhang the brows, with the exception of a small upright fringe behind the brows that meets the forward hairs in a small crest. The scrotum is rust-red.
Habitat. Much of the range of the Paraguayan Howler is in the cerrado of central Brazil and semi-arid caatinga forest scrub in north-eastern Brazil, where they use gallery and riparian forest and patches of seasonal semi-deciduous and deciduous forests (mesic Atlantic Forest, “cerradao,” and arboreal caatinga). In southern Rondonia, they are associated with highland savanna habitats and gallery forest in the Guaporé grasslands. In Paraguay, they occur in eastern forests and, in certain areas of the Chaco, gallery forests along the rios Paraguay and Pilcomayo and numerous small rivers draining the Chacoan plain. In Bolivia, they are found in riparian forest in the Chaco along the Rio Parapeti, the inundated and terra firma lowland and submontane dry Chiquitania forest. In the southern part ofits distribution, high numbers of Paraguayan Howlers occur in flooded (seasonally or irregularly) and highly productive riparian forest in the basins of the rios Parana and Paraguay in northern Argentina and the Pantanal in Bolivia and Mato Grosso, Brazil. Periodic flooding results in a continual deposition of alluvial sediments. The diversity of trees is not high; the flooding regime selects for those that can tolerate having their roots underwater for prolonged periods (occasional very prolonged floods can result in widespread die off of trees). A botanical survey of a 1-ha plot on the island of Brasilera in the Rio Parana, Argentina, contained just 23 tree species. The flora of these islandsis evidently not rich, but it is optimal for Paraguayan Howlers. Some populations in Argentina include pine plantations in their home ranges.
Food and Feeding. In a study by S. Bravo and A. Sallenave on the fluvial island of Brasilera, the annual diet of Paraguayan Howlers included parts of 22 plant species from 15 families, mainly fruits, leaves (young and mature), and flowers. Annually, mature leaves made up 51% ofthe diet,ripe fruits 19% (but as high as 71% in some months), young leaves 13%, flowers 13%, and buds 4%. Other items eaten in small quantities included petioles, buds, and aquatic plants. In the cerrado, Paraguayan Howlers eat roots of the marsh-living spikesedge Eleocharis (Cyperaceae), which are also a good source of water. When fruits, young leaves, or flowers were unavailable, they ate mature leaves, forming the large majority of the diet in May-July. It is possible that palatable mature leaves were a scarce commodity at this time, as evidenced by the groups splitting into two subgroups each day, coming together only in the late afternoon to sleep. Animal protein came from arthropods consumed with leaves (e.g. aphids or galls) or fruits such as Ocotea (Lauraceae) and Ficus (Moraceae). Figs contained galls inside their fruits. Each month, the principal food item of Paraguayan Howlers was heavily infested, and in the case of Ocotea, they evidently chose to feed from trees suffering from these infestations. Fruits of Ocotea diospyrifolia, for example, tended to be infested by curculionid beetles (weevils). Howlers ingesting these fruits kill parasitic beetles but do not harm seeds, which are effectively dispersed. Paraguayan Howlers feed more in the more infested trees, even going into a neighboring group’s home range to find them. Insect-infested food items accounted for ¢.25% of the diet during the year. These Paraguayan Howlers were living in very productive forests. In terra firma forests nearby, leaves can make up 70% of the annual diet. A year-long study of several populations of Paraguayan Howlers in north-eastern Argentina found that leaves made up 64-82% of the diet, fruits 12-19%, pine cones 6-7%, flowers 0-3%, bark 0-7%, and other items 0-1%. This is the only howler in which some populations feed on pine cones. They can also be seed predators. In Brazil, they open immature, oblong, woody pyxidia of Cariniana estrellensis (Lecythidaceae), picking them off the tree, and holding them so that they can bash them sideways, while raising the arm above the head to do so. After each strike, they look at the fruit to see if the operculum is open. When it is open, they pull it out and raise the pyxidium above their head and pour the seeds into their mouth. Howlers fed on these fruits at a time when other fruits and leaves were scarce, and males aggressively defended the tree against other howlers when feeding.
Breeding. Male Paraguayan Howlers reach sexual maturity at 24-37 months and females at 35-42 months. In captivity, females first reproduce at 35-42 months old. Gestation is ¢.180 days. The ovarian cycle is ¢.20 days. Annual birth rate in the wild in northern Argentina has been recorded at 0-89 infants/female/year. Births occur throughout the year in most populations, but they are seasonally facultative with extreme changes in food availability. In terra firma gallery forest in northern Argentina, conceptions tend to occur in the wet season when food is abundant, with births occurring in the dry season when food is scarce so that weaning is timed to coincide with food abundance (peaking in April-August). In flooded forest, however, food availability is much less seasonal, and births tend to occur throughout the year. Alloparental care is common. Males carry infants and helpjuveniles, and females suckle infants and even juveniles that are not their own. A case of adoption (the mother died) has also been recorded. Weaning occurs at 9-12 months. Interbirth intervals in captivity are 7-15-5 months, and in the wild, they average 15-9 months.
Activity patterns. Activity patterns of Paraguayan Howlers are extremely variable, depending on group size and food availability. They generally rest 46-77% of the day, travel 2-30%, feed 13-18%, engage in social activities 3-9%, and other behaviors 1-5%. In the study of groups on Brasilera Island, two groups rested 57% ofthe day, fed 19%, traveled 16%), engaged in social behaviors (mainly allogrooming and play) 6%, and confronted other groups 2%.
Movements, Home range and Social organization. Groups of Paraguayan Howlers are unimale-multifemale or multimale-multifemale, with 3-22 individuals. In general, groups are quite small, and high densities are often characterized by numerous small groups in small home ranges (2-4 ha). Groups are large in seasonal deciduous and semi-deciduous forests of islands in the Rio Parana in northern Argentina. They are believed to result from difficulties in dispersing in riparian forest islands and forest patches. Two groups studied on the island of Brasilera (Rio Parana) had 16 and 22 individuals: one with two adult males and five adult females and the other with two adult males and six adult females. In Brazil, between the rios Paranapanema and Ivinhema, 13 groups had 6-18 individuals (average 11-5), with 1-3 adult males. Seventeen groups on the island of Tragadero Sur also in the Rio Parana had 4-14 individuals, with 1-9 adult males and 1-5 adult females. In terra firma areas and especially dry forests, groups of Paraguayan Howlers tend to be smaller. At a site in the eastern Argentinean Chaco, seven groups had 2-10 individuals (average 5-7), with densities of 12-26 ind/ km? Home range size varies from less than 2 ha to 117 ha, with daily movements of 75-1666 m. In riparian forests of the Chaco in Kaa-lya del Gran Chaco National Park, Bolivia, densities were 15-187 ind/km?®. The density on the island of Brasilera in Argentina was very high at 425 ind/km?*. When home ranges are very small, daily movements are as low as 85 m but up to 1500 m, and group encounters are frequent, up to six a day. Both sexes disperse. Juvenile and subadult females spend some time on the periphery of their natal group’s home range before they are evicted by adult females that vocalize and threaten and chase them. Infanticide has been reported after a male enters a group and takes over as the dominant male. Females do not enter established groups, but form new groups with dispersing males in new territories. Females form a dominance hierarchy, with the youngest being the most dominant.
Status and Conservation. CITES Appendix II. Classified as Least Concern on The [UCN Red List. The Paraguayan Howler is a wide-ranging species and in some areas common. Nevertheless, over large expanses ofits distribution, populations have been reduced or lost as suitable habitat becomes highly fragmented due to conversion for farmland, including commercial plantations (tees and crops) and pasture. Enormous numbers of Paraguayan Howlers are lost when rivers are dammed. The Paraguayan Howler is wide-ranging and adaptable; in some regions, it can be found in small, semi-natural and degraded forests, able to thrive on cultivated species such as bamboos, eucalyptus, tangerines, peaches, guavas and timber trees such as Melia azedarach (Meliaceae) and Schizolobium parahyba (Fabaceae). They are generally not hunted for food (their flesh is considered bitter), but the plush of the male is much sought after by local people to make caps, bags, and blankets.
Bibliography. Agoramoorthy & Lohmann (1999), Agostini et al. (2008, 2010), Aguiar, Ludwig & Passos (2009), Aguiar, Mellek et al. (2007), Aguiar, Pie & Passos (2008), Anderson (1997), Bicca-Marques (1993, 1994, 2003b), Bicca-Marques & Calegaro-Marques (1994a, 1994b), Bicca-Marques, Muhle et al. (2009), Bicca-Marques, Prates et al. (2008), Bravo & Sallenave (2003), Bravo & Zunino (1998), Brown & Rumiz (1986), Calegaro-Marques & Bicca-Marques (1993, 1996), Codenotti et al. (2002), Di Fiore et al. (2011), Dvoskin et al. (2004), Gregorin (2006), Gregorin et al. (2008), Jones, C.B. (1983), Kowalewski & Garber (2010), Kowalewski & Zunino (2004), Oliveira-Filho & Galetti (1996), Pope (1966), Rodrigues & Marinho-Filho (1995), Rumiz (1990), Rumiz et al. (1986), Shoemaker (1982), Stallings (1985), Thorington et al. (1984), Villalba et al. (1995), Wallace & Rumiz (2010), Zunino (1996), Zunino et al. (2001).
description: Published as part of Russell A. Mittermeier, Anthony B. Rylands & Don E. Wilson, 2013, Atelidae, pp. 484-549 in Handbook of the Mammals of the World – Volume 3 Primates, Barcelona :Lynx Edicions on pages 531-532, DOI: 10.5281/zenodo.5727205