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Alouatta guariba

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Taxonomy [top]

Kingdom Phylum Class Order Family
ANIMALIA CHORDATA MAMMALIA PRIMATES ATELIDAE

Scientific Name: Alouatta guariba
Species Authority: (Humboldt, 1812)
Infra-specific Taxa Assessed:
Common Name/s:
English Brown Howler Monkey, Brown Howling Monkey, Southern Brown Howling Monkey
French Hurleur Brun
Spanish Barbado, Bugio, Guariba
Synonym/s:
Alouatta fusca (É. Geoffroy, 1812)
Taxonomic Notes: Rylands and Brandon (1998) and Gregorin (2006) discuss the validity or otherwise of the use of the alternative names of fusca and guariba for the Brown Howler Monkey of the Atlantic forest of Brazil and Argentina. Rylands and Brandon-Jones (1998) indicated that guariba Humboldt, 1812, is the available name, Gregorin (2006) that fusca E. Geoffroy, 1812, is the right name. Kinzey (1982; see also Rylands et al. 1996) described pelage variation. Gregorin (2006), studying the morphology of the cranium and hyoid apparatus, considered the two brown howlers, listed by Rylands et al. (2000) and Groves (2001, 2005) as subspecies, to be full species. We reserve judgment on this until genetic studies can be brought to bear. Harris et al. (2005), analysing cytochrome-b gene sequences, found significant differences between populations of A. guariba clamitans in southern Brazil—from Rio de Janeiro on the one hand and Santa Catarina on the other. They showed that these correspond to differences in karyotype recorded by Koiffman (1977), and Oliveira et al. (1995, 1998, 2002). Maximum genetic distances found by Harris et al. (2005) were considerably greater than those recorded for A. caraya and A. belzebul by Nascimento et al. (2005), and they argued that further genetic research may result in the recognition of three species of Brown Howler Monkey. We continue with the names and subspecific classification as used by Rylands et al. (2000) and Groves (2001, 2005) until their taxonomy becomes better defined.

Assessment Information [top]

Red List Category & Criteria: Least Concern ver 3.1
Year Published: 2008
Date Assessed: 2008-06-30
Assessor/s: Mendes, S.L., Rylands. A.B., Kierulff, M.C.M. & de Oliveira, M.M.
Reviewer/s: Mittermeier, R.A. & Rylands, A.B. (Primate Red List Authority)
Justification:
The species is listed as Least Concern because, although it occurs in the Atlantic Forest of Brazil, a region with a high rate of historical forest loss, it remains widely distributed, is present in many protected areas, and is not declining at a rate sufficient to qualify for a threat category.
History:
2003 Near Threatened
2003 Near Threatened (IUCN 2003)
2000 Vulnerable
1996 Vulnerable
1996 Vulnerable
1994 Vulnerable (Groombridge 1994)
1990 Vulnerable (IUCN 1990)
1988 Indeterminate (IUCN Conservation Monitoring Centre 1988)
1986 Indeterminate (IUCN Conservation Monitoring Centre 1986)
1982 Indeterminate (Thornback and Jenkins 1982)

Geographic Range [top]

Range Description: This species inhabits a large part of the Atlantic forest of Brazil, south from southern Bahia (formerly south from the Rio Paraguaçú), extending south into basin of the Rio Jacuí, municipality of São Lourenço do Sul, state of Rio Grande do Sul (Printes et al. 2001), and the extreme north of Argentina in the Department of Misiones (Crespo 1954; Rylands et al. 1988; Di Bitetti et al. 1994; Rylands 1994; Marques 2003). Aguiar et al. (2007) recorded sympatry and probable hybridization with A. caraya in riparian forest along the left margin of the Rio Paraná (between Porto Figueira and Port Camargo) in the Ilhas e Várzeas do Rio Paraná Environmental Preotection Area on the state of Paraná. This region is considered to be an ecotone between Cerrado (the typical domain of A. caraya) and the Atlantic forest (A. guariba).

Kinsey (1981) argued that the Rio Doce separated a northern subspecies (the nominate) from the southern subspecies (A. g. clamitans). However, through a large part north of the Rio Doce, howler monkeys were indistinguishable from those south (S. Mendes pers. comm.). Surveys by Rylands et al. (1988) resulted in the discovery of groups just south of the lower Jequitinhonha, which were all pale gold in colour, whereas further west, north of the middle Jequitinhonha, groups in dedicuous forests showed sexual dichromatism typical of clamitans further south (females dark brown, males golden brown). North of the Jequitinhonha, there are very few records of any Brown Howler Monkeys at all, and few significant populations remain. If the uniformly pale howlers of the lower Jequitinhonha are, in fact, a distinct subspecies (the nominate), then the populations can only be miniscule. But, the validity of the two subspecies remains doubtful, and confused even with a recent genetic analysis comparing populations in the south of its range in the states of Santa Catarina, Sao Paolo and Rio de Janeiro suggesting strong subpopulation differentiation in clamitans.
Countries:
Native:
Argentina (Misiones); Brazil (Bahia, Espírito Santo, Minas Gerais, Paraná, Rio de Janeiro, Rio Grande do Sul, Santa Catarina, São Paulo)
Range Map: Click here to open the map viewer and explore range.

Population [top]

Population: There have been a fair number of population estimates thorughout the range of this species. Most of them in very small forest fragments. González-Solís et al. (2001) provide a recent summary. They list 11 sites (forests) where brown howlers were counted, ranging from from 50 ha to 100,000 ha. Densities can be very high. When not hunted, densities can vary in even very small forests due to their folivory and dietary flexibility. In the 50 ha site (Lageadinho, São Paulo) group size was 6-12, and the density 98 individuals/km² (Torres de Assumpção 1983). Chiarello (1993) recorded a density of 177 individuals/km² at the Santa Genebre Reserve (259 ha), São Paulo. Estimates of densities at the Caratinga Biological Statiion (survey area ranging from 570 to 800 ha), Minas Gerais, have varied from 92 to 149 individuals/km² (Mendes 1985, 1989; Hirsch 1995). Lower densities, 10.1 individuals/km², were recorded in the Augusto Ruschi Biological Reserve (4,000 ha), Espírito Santo, by Pinto et al. (1993). Hirsch (1995) estimated densities of 1.8 to 49.0 individuals/km² in the Rio Doce State Park (32,210 ha), Minas Gerais. González-Solís et al. (2001) estimated a density of 0.79 individuals/km² in the Serra do Paranapiacaba, in four contiguous protected areas in the state of São Paulo totalling 140,000 ha (the state parks of Intervales, Turístico Alto Ribeira and Carlos Botelho, and the Xitué State Ecological Station). Surveys by Chiarello (1995) in the Linhares Forest Reserve, Espírito Santo failed to register howlers even though they were present. In later surveys in the same reserve, Chiarello (1999) recorded an encounter rate of 0.15 groups/10 km. Schneider and Marques (1999) estimated a density of 92-125 individuals/km² in the southern part of the range of this species, in mixed broadleaf/Araucaria forest in the Aracuri-Esmeralda Ecological Station. Buss (2001) estimated 65 to 85 individuals/km² in the Itapuã State Park.

Note that there have been quite a number of behavioural-ecological field studies of this species, and a number of density estimates available in the literature are a result of these studies. The study sites chosen were those where howler monkeys were found to be numerous and visible, so these high densities are undoubteldy at the top end of the densities possible for this species and do not reflect a situation typical of the entire range of the species. Where they are hunted they will occur in very much lower numbers or not at all. In some areas they are scarce even though hunting is minimal or absent (for example, the Rio Doce State Park, or the Augusto Ruschi Biological Station). The explanation for low population densities in these cases is generally sought in disease epidemics, especially yellow fever.

In Misiones, Argentina, densities of both A. guariba and A. caraya are extremely low probably as a result of the dramatic habitat fragmentation suffered in the last few decades, and of an older yellow fever outbreak that occurred in 1966.
Population Trend: Decreasing

Habitat and Ecology [top]

Habitat and Ecology: An inhabitant of lowland, submontane and montane forest of the Atlantic coast of Brazil, extending inland to mesophytic semideciduous seasonal forest inland in the states of São Paulo, Minas Gerais and Paraná (Rylands et al. 1988; Mendes 1985, 1989; Chiarello 1993, 1995, 1999; Marques 2001). In Paraná and Rio Grande do Sul, it occurs in the highly seasonal subtropical and temperate, mixed broadleaf/Araucaria forest (Schneider and Marques 1999; Buss 2001). Aguiar et al. (2007) recorded it in periodically flooded, seasonal, semideciduous forest in the floodplains of the Rio Paraná, Paraná.

The howler monkeys are the large leaf-eaters of the South American primate communities. The molar teeth are particularly adapted for chewing leaves through shearing. Like the spider monkeys, they are prehensile-tailed, with a naked patch of skin on the under surface at the tip. 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).

Brown Howler Monkeys an be seen in groups of four or five, but up to 11 or so, individuals. There is usually only one dominant male in the group (occasionally two), others being subordinate younger male, sub-adults, or juveniles, 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).

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.

Size:
Adult male weight mean 6.73 kg (n=4) (Smith and Jungers 1997)
Adult female weight mean 4.35 kg (n=5) (Smith and Jungers 1997).
Systems: Terrestrial

Threats [top]

Major Threat(s): Widespread forest loss and fragmentation throughout its range, hunting, and disease epidemics are the main threats. However, the species is able to survive in even quite small forest fragments if there is no hunting. Selective logging for prized Araucaria pine is a threat in the south of its range. Mortality has also been reported due to electrocution from power lines, mainly in the small populations surviving in urban parks such as Lami Municipal Reserve, Porto Alegre (Lokschin et al. 2007).

Conservation Actions [top]

Conservation Actions: This species is present in a number of protected areas:

Argentina
Cruce Caballero Provincial park (435 ha) (at least two groups, Di Bitteti et al. 1994; Parera 2002)
Urugua-í Provincial Park (Parera 2002)
Piñalito Natural Reserve (3,796 ha) (Parera 2002). (A. caraya also occurs in this park, between the Rios Uruguai and Paraná, and hybrids have been recorded there (Di Bitteti 2005). Di Bitetti (2005) suggested A. caraya was replacing A. guariba in ths region due to forest destruction and degradation).

Brazil

Espírito Santo
Linhares Forest Reserve (Companhia Vale do Rio Doce) (22,000 ha) (Mendes 1991; Chiarello 1995).
Augusto Ruschi Biological Reserve (3,572 ha) (Mendes, 1991; Pinto et al. 1993)
Sooretama Biological Reserve (27,943 ha) (rare, Chiarello 1999)
Córrego Grande Biological Station (1,489 ha)
Pedra Azul State Biological Reserve (1,200 ha) (Mendes 1991)
Duas Bocas State Biological Reserve (2,910 ha) (Mendes 1991)
Fazenda Montes Verdes Forest Reserve (1,500 ha) (Mendes 1991)
Santa Lúcia Biological Station (400 ha) (Mendes 1991)
São Lourenço Biological Station (22 ha) (Mendes 1991)

Minas Gerais
Caparaó National Park (across the Espírito Santo border) (31,853 ha)
Rio Doce State Park (35.973 ha) (Stallings and Robinson 1991; Hirsch 1995)
Serra do Brigadeiro State Park (13,210 ha) (Cosenza 1993)
Ibitipoca State Park (1,488 ha) (Hirsch et al. 1994)
Caratinga Biological Station RPPN Feliciano Abdala (Mendes 1985, 1989)

Paraná
Ilha Grande National Park (108,166 ha) (Aguiar et al. 2007)
Ilhas e Várzeas do Rio Paraná Environmental Protection Area (1,003,059 ha) (Aguiar et al. 2007)

Rio de Janeiro
Serra dos Órgãos National Park (10,527 ha)
Serra da Bocaina National Park (across border with São Paulo) (98,115 ha)
Itatiaia National Park (28,155 ha) (Diblasi-Filho and Borsoi Jr. 1983)
Tinguá Biologica Reserve (24.902 ha)
Poço das Antas Biological Reserve (5,065 ha)
Desengano State Park (22,500 ha)
Floresta da Cicuta State Area of Outstanding Ecological Interest (144 ha)

São Paulo
Turístico Alto Ribeira State Park (36,712 ha) (González-Solís et al. 2001)
Carlos Botelho State Park (37,644 ha) (González-Solís et al. 2001)
Morro do Diabo State Park (Coimbra Filho 1976b)
Serra do Mar State Park
Cantareira State Park (7,000 ha) (Cordeiro da Silva 1981; Oliveira and Ades 1993)
Paranapiacaba State Biological Reserve (336 ha)
Juréia-Itatins State Ecological Station (79,270 ha)
Xitué State Ecological Station (González-Solís et al. 2001)

Rio Grande do Sul
Aparados da Serra National Park (13,081 ha)
Itapuã State Park (5,566 ha) (Prates et al. 1990; Buss 2001; Marques 2003)
Espigão Alto State Park (1,319 ha) (Marques 2003)
Rondinha State Park (1,000 ha) (Marques 2003)
Turvo State Park (17,491 ha) (Marques 2003)
Serra Geral State Biological Reserve (4,846 ha) (Marques 2003)
Ibicuí-mirim Biological Reserve (598 ha) (Marques 2003)
Aracuri-Esmeralda Ecological Station (277 ha) (Marques 2003)
Lami Municipal Biological Reserve (Marques 2003)
São Francisco de Paula National Forest (1,607 ha) (Marques 2003)
Parque do Morro do Osso (Marques 2003)
Rota do Sol Environmental Protection Area (52,535 ha) (Marques 2003)

Argentina
Cruce Caballero Provincial park (435 ha) (at least two groups, Di Bitteti et al. 1994; Parera 2002)
Urugua-í Provincial Park (Parera 2002)
Piñalito Natural Reserve (Parera 2002). (A. caraya also occurs in this park, between the Rios Uruguai and Paraná, and hybrids have been recorded there [Di Bitteti 2005]. Di Bitetti (2005) suggested A. caraya was replacing A. guariba in ths region due to forest destruction and degradation).

It is listed on Appendix II of CITES.
Citation: Mendes, S.L., Rylands. A.B., Kierulff, M.C.M. & de Oliveira, M.M. 2008. Alouatta guariba. In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.2. <www.iucnredlist.org>. Downloaded on 19 April 2014.
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