Mastozoología Neotropical ISSN: 0327-9383 [email protected] Sociedad Argentina para el Estudio de los Mamíferos Argentina

Dias, Thomas D.; Conceição, Martha S.; Murer, Laurete; Fortes, Vanessa B. EXTENSION OF THE CONTACT ZONE AND PROBABLE HYBRIDIZATION BETWEEN BROWN HOWLER MONKEYS (Alouatta guariba clamitans) AND BLACKAND-GOLD HOWLER MONKEYS (Alouatta caraya) (, ) IN SOUTHERN Mastozoología Neotropical, vol. 22, núm. 2, 2015, pp. 303-310 Sociedad Argentina para el Estudio de los Mamíferos Tucumán, Argentina

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Artículo

EXTENSION OF THE CONTACT ZONE AND PROBABLE HYBRIDIZATION BETWEEN BROWN HOWLER MONKEYS (Alouatta guariba clamitans) AND BLACK- AND-GOLD HOWLER MONKEYS (Alouatta caraya) (PRIMATES, ATELIDAE) IN SOUTHERN BRAZIL

Thomas D. Dias1, Martha S. Conceição1, Laurete Murer2, and Vanessa B. Fortes 3

1 Laboratório de Primatologia, Universidade Federal de Santa Maria 2 Programa de Pós-Graduação em Medicina Veterinária, Centro de Ciências Rurais, Universidade Federal de Santa Maria. Camobi, Santa Maria, RS, Brasil 3 Laboratório de Primatologia, Centro de Educação Superior Norte do Rio Grande do Sul, Universidade Federal de Santa Maria, Av. Independência 3751, Bairro Vista Alegre, Palmeira das Missões, RS, Brasil, CEP 98.300-000. [Correspondence: Vanessa B. Fortes ]

ABSTRACT. Species of howler monkeys (genus Alouatta) generally are parapatric. However, many areas of sympatry between different species of this genus have been recorded in recent years. We report the discovery of a new contact zone and probable hybridization between black-and-gold howler monkeys (Alouatta caraya) and brown howler monkeys (Alouatta guariba clamitans) in São Vicente do Sul, Rio Grande do Sul, Brazil (29° 46’ 07” S; 54° 47’ 53” W). We report two sightings of heterospecific groups of black-and-gold and brown howler monkeys, each composed of eight individuals, including three probable hybrids (two subadult males and one adult female). We also observed monospecific groups of phenotypically pure individuals of both species. The most plausible explanation for the occurrence of this contact zone is that brown howlers may be using the riparian forest of the Ibicuí River and its tributaries as a dispersal route towards areas of the Pampa biome, typically inhabited by black-and-gold howlers.

RESUMEN. Extensión de la zona de contacto y probable hibridación entre monos aulladores marrones (Alouatta guariba clamitans) y monos aulladores negros y dorados (Alouatta caraya) (Primates, Atelidae) en el sur del Brasil. Las especies de monos aulladores (género Alouatta) generalmente se distribuyen de una manera parapátrica. Sin embargo, en los últimos años se han registrado muchas áreas de simpatría entre dis- tintas especies del género. En este estudio describimos el descubrimiento de una nueva zona de contacto y la probable hibridación entre monos aulladores negros y dorados (Alouatta caraya) y monos aulladores marrones (Alouatta guariba clamitans) en São Vicente do Sul, Rio Grande do Sul, Brasil (29° 46’ 07” S; 54° 47’ 53” W). Reportamos dos avistamientos de grupos heteroespecíficos de monos aulladores negros y dorados y marrones, cada uno de estos compuesto por ocho individuos, entre ellos tres híbridos probables (dos machos subadultos y una hembra adulta). También se observaron grupos monoespecíficos con individuos fenotípicamente puros de ambas especies. La explicación más plausible para la ocurrencia de esta zona de contacto es que los aulladores marrones están utilizando las matas ribereñas del río Ibicuí y sus afluentes como una ruta de dispersión hacia zonas del bioma Pampa, típicamente habitadas por aulladores negros y dorados.

Key words: Geographic range expansion. Hybrid zone. Mixed groups. Sympatry.

Palabras clave: Expansión de rango geográfico. Grupos mixtos. Simpatría. Zona híbrida

Recibido 2 noviembre 2014. Aceptado 22 mayo 2015. Editor asociado: M Kowalewski 304 Mastozoología Neotropical, 22(2):303-310, Mendoza, 2015 TD Dias et al. http://www.sarem.org.ar

INTRODUCTION Forest in the state of Paraná, Brazil (Aguiar et al., 2007) and at the northern boundary of The genus Alouatta is composed of 12 spe- the Pampa biome, very close to the Atlantic cies (Cortés-Ortiz et al., 2015) and is widely Forest sensu lato (Bicca-Marques et al., 2008). distributed in the Neotropics, occurring from At the contact zone of A. pigra and A. palliata 21º 17’ North (Yucatán, Mexico; Serio-Silva in the Mexican state of Tabasco, current forest et al., 2005) to 31º 10’ South (Rio Grande do fragmentation may have favored the increasing Sul, Brazil; Printes et al., 2001). In general, the proximity between individuals of these species, species are distributed parapatrically and are and promoted higher rates of interspecific isolated by barriers such as rivers, or by the crosses (Dias et al., 2013), and this may be preference/tolerance to different habitat types occurring in other areas where howler species (A. belzebul and A. caraya, Brazil: Chame and are sympatric too. Thus, further research on Olmos, 1997; A. seniculus and A. caraya, Bra- contact zones is needed to clarify which popu- zil: Iwanaga and Ferrari, 2002; A. palliata and lation and landscape attributes (either natural A. seniculus, Colombia: Defler, 2004;A. pigra or antropogenically produced) are likely to and A. palliata, Guatemala: Baumgarten and affect the process of natural hybridization and, Williamson, 2007). In recent years, however, consequently, the persistence of hybrid zones. many contact zones have been recorded, includ- Well-documented cases of natural hybridiza- ing those between A. pigra and A. palliata in tion among primates are not common, but they Mexico (Cortés-Ortiz et al., 2003), A. seniculus are of great importance for the understanding and A. sara in Bolivia (Büntge and Pyritz, 2007), of reproductive isolation (Cortés-Ortiz et al., A. seniculus and A. caraya in Bolivia (Wallace 2007) and the factors involved in the forma- et al., 2000), A. seniculus and A. belzebul in tion and maintenance of species (Arnold and Brazil (Pinto and Setz, 2000), and A. caraya Meyer, 2006). For example, the study of hybrids and A. guariba clamitans in Brazil (Aguiar et between A. pigra and A. palliata in the hybrid al., 2007; Bicca-Marques et al., 2008) and Ar- zone of Tabasco, Mexico (compared to purebred gentina (Agostini et al., 2008). The occurrence individuals in different areas) allowed research- of heterospecific groups with putative hybrids ers to tease apart the effects of genetics, social is only known in four of these areas (Aguiar et structure and environmental factors on the al., 2007; Cortés-Ortiz et al., 2007; Agostini et behavior of the studied , and revealed al., 2008; Bicca-Marques et al., 2008). ancestry as an important determinant of the Black-and-gold howlers (A. caraya) and female social behavior (Ho et al., 2014). The brown howlers (A. guariba clamitans) com- study of hybrids also can clarify the mecha- monly occupy distinct biomes. Black-and-gold nisms that limit the adaptation of species and howlers inhabit bush savanna and dry forests, the expansion of their geographical distribution humid forests (brejos), semi-deciduous and (Holt et al., 2005; Bridle and Vines, 2007). This deciduous forests, gallery forests, and flooded study aims to report the discovery of a new forests, mainly in the Cerrado, Pantanal, Chaco, contact zone and the probable hybridization and Pampa biomes (but also in the Brazilian between A. caraya and A. guariba clamitans Caatinga, see Chame and Olmos, 1997), in in São Vicente do Sul, Rio Grande do Sul, Brazil, Argentina, Paraguay and Bolivia (Brown Brazil, which extends the southern boundary of and Zunino, 1994; Zunino et al., 1996, 2001; sympatry between these species and, possibly, Hirsch et al., 2013; IUCN, 2013). Brown howl- the limit of the hybrid zone. ers typically occur in the Brazilian Atlantic Forest, which extends to Misiones in Argentina METHODS (Hirsch et al., 2013; Di Bitetti, 2005). There are records of sympatry between black-and- Heterospecific groups of howler monkeys were gold and brown howlers in areas of Araucaria detected at Estância Defesa (29o49’04.33”S; forest in Argentina (Agostini et al., 2008), at 54o47’29.97”W; 146 m AMSL), a particular area the ecotone between Cerrado and Atlantic located in the Pampa Biome, more precisely in the CONTACT ZONE OF HOWLER MONKEYS IN SOUTHERN BRAZIL 305

municipality of São Vicente do Sul (Fig. 1), in the adult male, adult female, juvenile or infant) based state of Rio Grande do Sul, Brazil. The area includes on criteria adopted by Rumiz (1990) for A. caraya 200 ha of riparian forest on the margins of the and by Mendes (1985) for A. guariba clamitans. We Ibicuí River and its tributaries, and is composed by were not able to assure whether or not immature seasonal tree species (IBGE, 2004). The climate in individuals presenting a pelage concordant with the area is humid subtemperate, with average annual A. caraya (golden) were putative hybrids, because the temperatures of 18-22 °C and average temperatures typical hybrid coloration (Gregorin, 2006; Aguiar et under 13 °C during the colder months, with four al., 2007, 2008; Agostini et al., 2008; Bicca-Marques well-defined seasons due to circannual variation in et al., 2008) will only be apparent in subadult or temperature and photoperiod (Maluf, 2000). adult (black) males. We took about 30 min. to count From January 2011 to November 2012, T. D. Dias and identify all individuals in each group. All indi- conducted a survey of medium-sized terrestrial viduals were photographed and the sightings were in the study area (transects covered on foot geo-referenced using a hand-held Global Positioning between 18:00 and 00:00 h, recording sightings and System (GPS) Garmin E-trex H. vestiges-feces, footprints) (Dias, 2012). During that study, groups of howlers (including a heteroespecific RESULTS group) were eventually sighted. On October 20th, 2013, we conducted an expedition aimed specifi- We obtained two records of heterospecific cally at locating howler groups, verifying if there groups in the study area (Table 1), but given were other mixed groups, and observing/recording the proximity of the coordinates, and the time in detail the patterns of coloration of the putative difference between records, it is possible that hybrids. In this expedition we searched for groups it was only one group, whose composition in a small stretch of the riparian zone of the Ibicuí changed from one year to another. We sighted River (15:30 to 17:00 h), and one of its tributaries the first heterospecific group in July 2012, and (9:30 to 15:00 h). Every time we sighted a group of howlers we it was composed by one adult male, two adult recorded the number of individuals, and their spe- females and one juvenile male A. caraya, and cies (or putative hybrid condition) based on patterns one adult male and one adult female A. guariba of coloration (Gregorin, 2006). We assigned each clamitans. This latter female was dorsally car- individual to an age-sex category (adult male, sub- rying an infant of undetermined sex, whose

Fig. 1. Location of Alouatta guariba clamitans groups, Alouatta caraya groups, and mixed groups in the study area (Estância Defesa), in São Vicente do Sul, RS, Brazil. 306 Mastozoología Neotropical, 22(2):303-310, Mendoza, 2015 TD Dias et al. http://www.sarem.org.ar

Table 1 Howler groups recorded in the study area, with their respective composition. ADM: adult male; SADM: subadult male; ADF: adult female; JUV: juvenile; INF: infant; NI: not identified; IM: immatures (infants + juveniles).

Date Group Coordinates ADM SADM ADF JUV INF NI of Record Size A.caraya March 2011 29°46’04”S; 54°47’49”W 1 1 1 3 A. guariba June 2012 29°46’04”S; 54°47’49”W 1 2 1 4 A. guariba October 2013 29°49’38”S; 54°44’56”W 1 2 1 1 5 Mixed July 2012 29°46’04”S; 54°47’49”W 1Ac, 1Ag 1Hy 2Ac, 1Ag 1Ac? 1Ac? 8 Mixed October 2013 29°46’07”S; 54°47’53”W 1Ac 1Hy 1Ac, 1Ag, 1Hy 3Ac? 8

Ac = Alouatta caraya, Ag = Alouatta guariba clamitans, Hy = putative hybrid, ? = immature coloration does not allow to identify whether or not hybrids are possible.

coloration was consistent with that of A. caraya (Bicca-Marques et al., 2008; Cortés-Ortiz et (that infant was photographed some months al., 2015). later, as a juvenile, showed in Fig. 2a). The group also had a subadult male with black DISCUSSION pelage and brown-red highlights on its back and head (Fig. 2b), possibly a hybrid. The Hybridization in primates is well documented second recording of a heterospecific group was for a few taxa (Cortés-Ortiz et al., 2007, 2015). obtained in 2013, and consisted of an adult As in African cercopithecines (Papio, Cercopi- male, an adult female and three juveniles (two thecus) (Detwiler et al., 2005), anthropogenic males and one juvenile of undetermined sex), habitat fragmentation may increase the inci- all of them with coloration concordant with A. dence of hybridization in howler monkeys, caraya; one subadult male with black pelage and because the confinement of a few individuals red highlights on its head and back (Fig. 3b); in small fragments can reduce the chances of a female whose coloration was typical of A. finding conspecific partners, which can lead guariba clamitans and a brown-colored adult to more frequent contact with groups of other female, with lighter fur on the tail, external species, and to interspecific crosses (Dias et part of the thighs, arms, head and back (Fig. al., 2013). The landscape in our study site is 3a). Hybrids are suspected to occur in those naturally fragmented (the municipality of São groups based on similarities in color patterns as Vicente do Sul presents 527.71 km2 of grass- described by Aguiar et al. (2007, 2008), Bicca- lands, and only 97.88 km2 of forested habitats), Marques et al. (2008) and Gregorin (2006). and there are no records of extensive deforesta- Monospecific groups of pure individuals of tion in recent times (UFRGS/EMBRAPA, 2007). both species were also recorded in the study This landscape configuration may increase the area (Table 1). Two of these records were taken chances of hybridization, in part because of the in near proximity to mixed groups, but only risks associated with long distance dispersal that one A. guariba clamitans group was found in may be required to find conspecifics (see the the riparian forest of the Ibicuí river (29° 49’ case of Cercopithecus cephus and Cercopithecus 38” S; 54° 44’ 57” W), at a greater distance nictitans in the Lopé Reserve, Gabon; Detwiler from the mixed groups (Fig. 4). Besides, our et al., 2005). In our study site the narrow strips record of heterospecific howler groups with of riparian forest that remain may hamper putative hybrids is located near 30 km south howlers’ displacements. from Cerro dos Negros, the southernmost The study site is located exclusively within limit for this contact zone until this date the Pampa biome, which is tipically inhabited CONTACT ZONE OF HOWLER MONKEYS IN SOUTHERN BRAZIL 307

Fig. 2. Putative hybrids observed in 2011/2012: (a) Juvenile Fig. 3. Putative hybrids observed in 2013: (a) adult female showing a coloration concordant with Alouatta caraya, with brown coloration, but with lighter fur on the tail, besides its possible mother (on the left), which had typical the external part of the thighs, arms, head and back; (b) Alouatta guariba clamitans fur; (b) Subadult male with black subadult male with black coloration and red highlights on coloration and red highlights on its head and back (on the head and back . right), besides an adult male with typical coloration of A. caraya (on the left). by A. caraya (Fig. 5), but the headwaters of The sizes of the groups recorded in our the Ibicuí River are located in areas of seasonal study site were smaller than in nearby areas. deciduous forest (Atlantic Forest sensu lato) The monospecific group ofA. caraya had only on the southern foothills of the geological three individuals, smaller than the three groups formation known as Serra Geral (Leite and (with 5, 10, and 15 individuals) recorded by Klein, 1990), typically inhabited by A. guariba Bicca-Marques et al. (2008) in São Francisco clamitans (Fig. 5). Thus,A. guariba clamitans de Assis (30 km to the northwest), and groups may be using the riparian forest of the Ibicuí of A. guariba clamitans had only 4 or 5 indi- River and tributaries as a dispersal route from viduals versus the average 5.8 (± 2.2) in Santa the seasonal forest toward areas of the Pampa. Maria (90 km to the east; Fortes, 2008) and As in other contact zones of A. caraya and 7 individuals in a single group observed in A. guariba clamitans, the presence of both São Francisco de Assis (Bicca-Marques et al., howler species in our study site is compatible 2008). Heterospecific groups in this study were with a secondary contact (Cortés-Ortiz et al., slightly larger than the average group size for 2015), promoted by the recent expansion of A. guariba clamitans (6.9 ± 2.0 individuals, n = 3 gallery forests in this area (Bicca-Marques et groups in 17 study sites; Fortes et al., 2015), al., 2008). but smaller than the average size for A. caraya 308 Mastozoología Neotropical, 22(2):303-310, Mendoza, 2015 TD Dias et al. http://www.sarem.org.ar

Fig. 4. Individuals of pure Alouatta guariba clamitans group on the Ibicuí river banks, São Vicente do Sul, RS, Brazil: (a) adult female; (b) adult male.

groups (9.8 ± 5.3 individuals, n = 15 groups in 11 study sites; Fortes et al., 2015). Their sex composition is more similar to that of A. caraya groups, which are composed of one adult and two subadult males (Di Fiore and Campbell, 2007), whereas groups of A. guariba clamitans in nearby areas typi- cally have a single male (Bicca-Marques et al., 2008; Fortes, 2008). The size and com- position of the groups in the contact zone may be an important determinant of the outcome of competition between mixed and pure groups (Dias et al., 2013). This is a topic for future investigation. At the edges of the geographic range, populations are usually smaller and more fragmented (lower population densities) than in the core area of the species dis- tribution (Brown et al., 1995; Thomas and Kunin, 1999). Thus, heterospecific groups

Fig. 5. Occurrence of Alouatta caraya (black dots) and Alouatta guariba clamitans (white dots) in the state of Rio Grande do Sul, Brazil (Font: Fundação Zoobotânica do Rio Grande do Sul/Secretaria de Meio Ambiente do estado do Rio Grande do Sul, unpublished database used for the last assessment of of these species in the state). Detailed map shows the location of the southernmost record of sympatry prior to this study (Bicca-Marques et al., 2008), and the points where pure and mixed groups were recorded in this study (black and white squares). The approximate boundary between the physiognomy of seasonal deciduous forest to the north and the Pampa to the south is given by the white line. CONTACT ZONE OF HOWLER MONKEYS IN SOUTHERN BRAZIL 309 could be formed as result of the Allee ef- zone, State of Rio Grande do Sul, Brazil: Evidence fect—low abundance or unbalanced sex ratios for hybridization. Primates 49:246-252. BRIDLE JR and TH VINES. 2007. Limits to evolution at lead to a difficulty to find conspecific sexual range margins: When and why does adaptation fail? partners (Courchamp et al., 1999; Stephens and Trends in Ecology and Evolution 22:140-147. Sutherland, 1999). This could be the case in El BROWN AD and GE ZUNINO. 1994. Hábitat, densidad Piñalito Provincial Park, Misiones, Argentina, y problemas de conservacion de los primates de Argentina. Vida Silvestre Neotropical 3:30-40. where A. caraya individuals seem to be spread- BROWN JH, DW MEHLMAN, and GC STEVENS. 1995. ing into areas typically inhabited by A. guariba, Spatial variation in abundance. Ecology 76: 2028-2043. or at São Francisco de Assis, Rio Grande do BÜNTGE ABS and LW PYRITZ. 2007. Sympatric Sul, Brazil, where A. guariba clamitans groups occurrence of Alouatta caraya and Alouatta sara at the río Yacuma in the Beni Department, northern decrease westwards, whereas the opposite trend Bolivia. Neotropical Primates 14:82-83. occurs for A. caraya groups (Cortés-Ortiz et al., CHAME M and F OLMOS. 1997. Two howler species in 2015). However, confirmation of this hypothesis southern Piauí, Brazil? Neotropical Primates 5:74-77. requires additional data on the density of both CORTÉS-ORTIZ L, E BERMINGHAM, C RICO, E RODRÍGEZ-LUNA, I SAMPAIO, and M RUIZ- species in this and other areas. GARCÍA. 2003. Molecular systematics and biogeography The coloration patterns of putative hybrid of the Neotropical monkey genus Alouatta. Molecular individuals indicate that there may be both male Phylogenetics and Evolution 26:64-81. and female hybrids in this area, as recorded CORTÉS-ORTIZ L, FTJ DUDA, D CANALES-ESPINOSA, F GARCÍA-ORDUÑA, E RODRÍGUEZ-LUNA, and in the upper Paraná River, Brazil (Aguiar et E BERMINGHAM. 2007. Hybridization in large- al., 2008), but genetic studies are needed to bodied new world primates. Genetics 176:2421-2425. confirm and further characterize suspected CORTÉS-ORTIZ L, I AGOSTINI, LM AGUIAR, hybridization. Additionally, demographic and M KELAITA, FE SILVA, and JC BICCA-MARQUES. 2015. Hybridization in howler monkeys. In: Howler behavioral studies in this area are also desir- Monkeys: Examining the Evolution, Physiology, able, aimed at a more comprehensive analysis Behavior, Ecology and Conservation of The Most of the mechanisms that promote or maintain Widely Distributed Neotropical . Pp. 107- hybridization in howler monkeys. 131, in: Developments in Primatology: Progress and Prospects (MM Kowalewski, PA Garber, L Cortés- Ortiz, B Urbani, and D Youlatos, eds.). Springer. LITERATURE CITED COURCHAMP F, T CLUTTON-BROCK, and B GRENFELL. 1999. Inverse density dependence and the Allee effect. AGOSTINI I, I HOLZMANN, and MS DI BITETTI. 2008. Trends in Ecology and Evolution 14:405-410. Infant hybrids in a newly formed mixed-species group DEFLER TR. 2004. Primates of Colombia. Conservation of howler monkeys (Alouatta guariba clamitans and International, Bogotá. Pp. 550, In: Tropical field guide Alouatta caraya) in northeastern Argentina. Primates series 5 (JV Rodríguez-Mahecha, A Rylands, and 49:304-307. RA Mittermeier, eds.). Bogotá, Colombia. AGUIAR LM, DM MELLEK, KC ABREU, TG BOSCARATO, DETWILER KM, AS BURRELL, and CJ JOLLY. 2005. IP BERNARDI, JMD MIRANDA, and FC PASSOS. Conservation implications of hybridization in African 2007. Sympatry between Alouatta caraya and Alouatta cercopithecinae monkeys. International Journal of clamitans and the rediscovery of free-ranging potential Primatology 26:661-684. hybrids in Southern Brazil. Primates 48:245-248. DIAS PAD, D ALVARADO-SERRANO, A RANGEL- AGUIAR LM, MR PIE, and FC PASSOS. 2008. Wild mixed NEGRÍN, D CANALES-ESPINOSA, and L CORTÉS- groups of howler species (Alouatta caraya and Alouatta ORTIZ. 2013. Landscape attributes affecting the clamitans) and new evidence for their hybridization. natural hybridization of Mexican howler monkeys. Primates 49:149-152. Pp. 423-435, in: Primates in Fragments: Complexity ARNOLD ML and A MEYER. 2006. Natural hybridization and Resilience (LK Marsh and CA Chapman, eds.). in primates: One evolutionary mechanism. Zoology Developments in Primatology: Progress and Prospects. 109:261-276. Springer, New York. BAUMGARTEN A and GB WILLIAMSON. 2007. DIAS TD. 2012. Comunidades de Mamíferos de Pequeno, Distribution of the monkey (Alouatta Médio e Grande Porte em Fitofisionomias Pampianas: pigra) and the mantled (Alouatta diversidade e uso de habitat. Trabalho de Conclusão palliata) in their contact zone in eastern Guatemala. de Curso. Universidade Federal do Pampa, São Neotropical Primates 14:11-18. Gabriel. 32 pp. BICCA-MARQUES JC, HM PRATES, FRC AGUIAR, DI BITETTI MS. 2005. Perspectivas para a conservação and CB JONES. 2008. Survey of Alouatta caraya, the de primatas em Misiones. Pp. 194-199, in: Mata black-and-gold howler monkey, and Alouatta guariba Atlântica: Biodiversidade, Ameaças e Perspectivas. clamitans, the brown howler monkey, in a contact (C Galindo-Leal and IG Câmara, eds.). Fundação SOS 310 Mastozoología Neotropical, 22(2):303-310, Mendoza, 2015 TD Dias et al. http://www.sarem.org.ar

Mata Atlântica, São Paulo, Conservação Internacional, MALUF RTJ. 2000. Nova classificação climática do Belo Horizonte. Estado do Rio Grande do Sul. Revista Brasileira de DI FIORE A and CJ CAMPBELL. 2007. The atelines: Agrometeorologia 8:141-150. Variation in ecology, behavior, and social organization. MENDES SL. 1985. Uso do espaço, padrões de atividades Pp. 155-185, in: Primates in Perspective (CJ Campbell, diárias e organização social de Alouatta fusca A Fuentes, KC MacKinnon, M Panger, and SK Beader, (Primates, Cebidae) em Caratinga, MG. MSc eds.). Oxford University Press, New York. dissertation, Universidade de Brasília, Brasília, Brazil FORTES VB. 2008. Ecologia e comportamento do bugio- PINTO LP and EZF SETZ. 2000. Sympatry and new ruivo (Alouatta guariba clamitans Cabrera, 1940) em locatlity for Alouatta belzebul discolor and Alouatta fragmentos florestais na Depressão Central do Rio seniculus in the Southern Amazon. Neotropical Grande do Sul, Brasil. Tese de Doutorado. Universidade Primates 8:150-151. Federal de Santa Maria, Santa Maria, Brasil. PRINTES RC, MV LIESENFELD, and L JERUSALINSKI. FORTES VB, JC BICCA-MARQUES, B URBANI, 2001. Alouatta guariba clamitans Cabrera, 1940: A VA FERNÁNDEZ, and TS PEREIRA. 2015. Ranging new southern limit for the species and for Neotropical behavior and spatial cognition of howler monkeys. primates. Neotropical Primates 9:118-121. Pp. 219-255, in: Howler Monkeys: Behavior, ecology RUMIZ DI. 1990. Alouatta caraya: Population density and and conservation (MM Kowalewski, PA Garber, L demography in Northern Argentina. American Journal Cortés-Ortiz, B Urbani, and D Youlatos, eds.). Springer, of Primatology 21:279-294. New York. SERIO-SILVA JC, V RICO-GRAY, and G RAMOS- GREGORIN R. 2006. Taxonomia e Variação Geográfica FERNÁNDEZ. 2005. Mapping primate populations das Espécies do Gênero Alouatta Lacépède (Primates: in the Yucatán peninsula, México: A first assessment. Atelidae) no Brasil. Revista Brasileira de Zoologia Pp. 489-511, in: New Perspectives in the Study 23:64-144. of Mesoamerican Primates: Distribution, ecology, HIRSCH AD, LG DIAS, LO MARTINS, RF CAMPOS, behavior, and conservation (A Estrada, PA Garber, NAT RESENDE, and EC LANDAU. 2013. Database MSM Pavelka, and L Luecke, eds.). Springer, New York. of georeferenced occurrence localities of Neotropical STEPHENS PA and WJ SUTHERLAND. 1999. primates. http://www.icb.ufmg. br/zoo/primatas/ Consequences of the Allee effect for behaviour, ecology bdp_tsspbiome.htm. and conservation. Tree 14:401-405. HO L, L CORTÉS-ORTIZ, PAD DIAS, D CANALES- THOMAS CD and WE KUNIN. 1999. The spatial structure ESPINOSA, DM KITCHEN, and TJ BERGMAN. 2014. of populations. Journal of Ecology 68: 647-657. Effect of ancestry on behavioral variation in two species UFRGS (Universidade Federal do Rio Grande do of howler monkeys (A. pigra and A. palliata) and their Sul)/EMBRAPA (Empresa Brasileira de Pesquisa hybrids. American Journal of Primatology 76:855-867. Agropecuária) Clima Temperado e Pecuária Sul. HOLT RD, TH KEITT, MA LEWIS, BA MAURER, and 2007. PROBIO: Cobertura Vegetal do Bioma Pampa ML TAPER. 2005. Theoretical models of species’ (Relatório técnico). Ministério do Meio Ambiente/ borders: Single species approaches. Oikos 108:18-27. Secretaria de Biodiversidade e Florestas, Brasília. 31 p. IBGE. Instituto Brasileiro de Geografia e Estatística. 2004. WALLACE RB, LRE PAINTER, DI RUMIZ, and Mapa da Vegetação do Brasil e Mapa de Biomas do AB TABER. 2000. Primate diversity, distribution and Brasil. http://www.ibge.gov.br. relative abundances in the Rios Blanco y Negro Wildlife IUCN Red List of Threatened Species. 2013. www. Reserve, Santa Cruz Department, Bolivia. Neotropical iucnredlist.org. Primates 8:24-2. IWANAGA S and SF FERRARI. 2002. Geographic ZUNINO GE, S BRAVO, FM FERREIRA, and distribution of red howlers (Alouatta seniculus) in C REISENMANN. 1996. Characteristics of two types southwestern Brazilian Amazonia, with notes on of habitat and the status of the howler monkey Alouatta caraya. International Journal of Primatology (Alouatta caraya) in northern Argentina. Neotropical 23:1245–1256. Primates 4:48-50. EITE PF, and RM KLEIN. 1990. Vegetação. Pp. 113-150, ZUNINO GE, V GONZÁLEZ, MM KOWALEWSKI, and in: Geografia do Brasil: Região Sul. V. 2. Instituto SP BRAVO. 2001. Alouatta caraya: Relations among Brasileiro de Geografia e Estatística, Rio de Janeiro. habitat, density, and social organization. Primate Report 61: 37-46.