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(Alouatta Guariba Clamitans) and BLACKAND-GOLD HOWLER MONKEYS (Alouatta Caraya) (PRIMATES, ATELIDAE) in SOUTHERN BRAZIL Mastozoología Neotropical, Vol

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(Alouatta Guariba Clamitans) and BLACKAND-GOLD HOWLER MONKEYS (Alouatta Caraya) (PRIMATES, ATELIDAE) in SOUTHERN BRAZIL Mastozoología Neotropical, Vol 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) (PRIMATES, ATELIDAE) IN SOUTHERN BRAZIL Mastozoología Neotropical, vol. 22, núm. 2, 2015, pp. 303-310 Sociedad Argentina para el Estudio de los Mamíferos Tucumán, Argentina Available in: http://www.redalyc.org/articulo.oa?id=45743273008 How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative Mastozoología Neotropical, 22(2):303-310, Mendoza, 2015 Copyright ©SAREM, 2015 Versión impresa ISSN 0327-9383 http://www.sarem.org.ar Versión on-line ISSN 1666-0536 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 <[email protected]>] 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 animals, 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,
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