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Extension de la zona de contacto y probable hibridacion entre monos aulladores marrones (Alouatta guariba clamitans) y monos aulladores negros y dorados (Alouatta caraya) (Primates, Atelidae) en el sur del Brasil.



The genus Alouatta is composed of 12 species (Cortes-Ortiz et al., 2015) and is widely distributed in the Neotropics, occurring from 21[degrees] 17' North (Yucatan, Mexico; Serio-Silva et al., 2005) to 31[degrees] 10' South (Rio Grande do Sul, Brazil; Printes et al., 2001). In general, the species are distributed parapatrically and are isolated by barriers such as rivers, or by the preference/tolerance to different habitat types (A. belzebul and A. caraya, Brazil: Chame and Olmos, 1997; A. seniculus and A. caraya, Brazil: Iwanaga and Ferrari, 2002; A. palliata and A. seniculus, Colombia: Defler, 2004; A. pigra and A. palliata, Guatemala: Baumgarten and Williamson, 2007). In recent years, however, many contact zones have been recorded, including those between A. pigra and A. palliata in Mexico (Cortes-Ortiz et al., 2003), A. seniculus and A. sara in Bolivia (Buntge and Pyritz, 2007), A. seniculus and A. caraya in Bolivia (Wallace et al., 2000), A. seniculus and A. belzebul in Brazil (Pinto and Setz, 2000), and A. caraya and A. guariba clamitans in Brazil (Aguiar et al., 2007; Bicca-Marques et al., 2008) and Argentina (Agostini et al., 2008). The occurrence of heterospecific groups with putative hybrids is only known in four of these areas (Aguiar et al., 2007; Cortes-Ortiz et al., 2007; Agostini et al., 2008; Bicca-Marques et al., 2008).

Black-and-gold howlers (A. caraya) and brown howlers (A. guariba clamitans) commonly occupy distinct biomes. Black-and-gold howlers inhabit bush savanna and dry forests, humid forests (brejos), semi-deciduous and deciduous forests, gallery forests, and flooded forests, mainly in the Cerrado, Pantanal, Chaco, and Pampa biomes (but also in the Brazilian Caatinga, see Chame and Olmos, 1997), in Brazil, Argentina, Paraguay and Bolivia (Brown and Zunino, 1994; Zunino et al., 1996, 2001; Hirsch et al., 2013; IUCN, 2013). Brown howlers typically occur in the Brazilian Atlantic Forest, which extends to Misiones in Argentina (Hirsch et al., 2013; Di Bitetti, 2005). There are records of sympatry between black-and- gold and brown howlers in areas of Araucaria forest in Argentina (Agostini et al., 2008), at the ecotone between Cerrado and Atlantic Forest in the state of Parana, Brazil (Aguiar et al., 2007) and at the northern boundary of the Pampa biome, very close to the Atlantic Forest sensu lato (Bicca-Marques et al., 2008). At the contact zone of A. pigra and A. palliata in the Mexican state of Tabasco, current forest fragmentation may have favored the increasing proximity between individuals of these species, and promoted higher rates of interspecific crosses (Dias et al., 2013), and this may be occurring in other areas where howler species are sympatric too. Thus, further research on contact zones is needed to clarify which population and landscape attributes (either natural or antropogenically produced) are likely to affect the process of natural hybridization and, consequently, the persistence of hybrid zones.

Well-documented cases of natural hybridization among primates are not common, but they are of great importance for the understanding of reproductive isolation (Cortes-Ortiz et al., 2007) and the factors involved in the formation and maintenance of species (Arnold and Meyer, 2006). For example, the study of hybrids between A. pigra and A. palliata in the hybrid zone of Tabasco, Mexico (compared to purebred individuals in different areas) allowed researchers to tease apart the effects of genetics, social structure and environmental factors on the behavior of the studied animals, and revealed ancestry as an important determinant of the female social behavior (Ho et al., 2014). The study of hybrids also can clarify the mechanisms that limit the adaptation of species and the expansion of their geographical distribution (Holt et al., 2005; Bridle and Vines, 2007). This study aims to report the discovery of a new contact zone and the probable hybridization between A. caraya and A. guariba clamitans in Sao Vicente do Sul, Rio Grande do Sul, Brazil, which extends the southern boundary of sympatry between these species and, possibly, the limit of the hybrid zone.


Heterospecific groups of howler monkeys were detected at Estancia Defesa (29[degrees] 49'04.33"S; 54[degrees] 47'29.97"W; 146 m AMSL), a particular area located in the Pampa Biome, more precisely in the municipality of Sao Vicente do Sul (Fig. 1), in the state of Rio Grande do Sul, Brazil. The area includes 200 ha of riparian forest on the margins of the Ibicui River and its tributaries, and is composed by seasonal tree species (IBGE, 2004). The climate in the area is humid subtemperate, with average annual temperatures of 18-22[degrees]C and average temperatures under 13[degrees]C during the colder months, with four well-defined seasons due to circannual variation in temperature and photoperiod (Maluf, 2000).

From January 2011 to November 2012, T D. Dias conducted a survey of medium-sized terrestrial mammals in the study area (transects covered on foot between 18:00 and 00:00 h, recording sightings and vestiges-feces, footprints) (Dias, 2012). During that study, groups of howlers (including a heteroespecific group) were eventually sighted. On October 20th, 2013, we conducted an expedition aimed specifically at locating howler groups, verifying if there were other mixed groups, and observing/recording in detail the patterns of coloration of the putative hybrids. In this expedition we searched for groups in a small stretch of the riparian zone of the Ibicui River (15:30 to 17:00 h), and one of its tributaries (9:30 to 15:00 h).

Every time we sighted a group of howlers we recorded the number of individuals, and their species (or putative hybrid condition) based on patterns of coloration (Gregorin, 2006). We assigned each individual to an age-sex category (adult male, sub-adult male, adult female, juvenile or infant) based on criteria adopted by Rumiz (1990) for A. caraya and by Mendes (1985) for A. guariba clamitans. We were not able to assure whether or not immature individuals presenting a pelage concordant with A. caraya (golden) were putative hybrids, because the typical hybrid coloration (Gregorin, 2006; Aguiar et al., 2007, 2008; Agostini et al., 2008; Bicca-Marques et al., 2008) will only be apparent in subadult or adult (black) males. We took about 30 min. to count and identify all individuals in each group. All individuals were photographed and the sightings were georeferenced using a hand-held Global Positioning System (GPS) Garmin E-trex H.



We obtained two records of heterospecific groups in the study area (Table 1), but given the proximity of the coordinates, and the time difference between records, it is possible that it was only one group, whose composition changed from one year to another. We sighted the first heterospecific group in July 2012, and it was composed by one adult male, two adult females and one juvenile male A. caraya, and one adult male and one adult female A. guariba clamitans. This latter female was dorsally carrying an infant of undetermined sex, whose coloration was consistent with that of A. caraya (that infant was photographed some months later, as a juvenile, showed in Fig. 2a). The group also had a subadult male with black pelage and brown-red highlights on its back and head (Fig. 2b), possibly a hybrid. The second recording of a heterospecific group was obtained in 2013, and consisted of an adult male, an adult female and three juveniles (two males and one juvenile of undetermined sex), all of them with coloration concordant with A. caraya; one subadult male with black pelage and red highlights on its head and back (Fig. 3b); a female whose coloration was typical of A. guariba clamitans and a brown-colored adult female, with lighter fur on the tail, external part of the thighs, arms, head and back (Fig. 3a). Hybrids are suspected to occur in those groups based on similarities in color patterns as described by Aguiar et al. (2007, 2008), Bicca- Marques et al. (2008) and Gregorin (2006).

Monospecific groups of pure individuals of both species were also recorded in the study area (Table 1). Two of these records were taken in near proximity to mixed groups, but only one A. guariba clamitans group was found in the riparian forest of the Ibicui river (29[degrees] 49' 38" S; 54[degrees] 44' 57" W), at a greater distance from the mixed groups (Fig. 4). Besides, our record of heterospecific howler groups with putative hybrids is located near 30 km south from Cerro dos Negros, the southernmost limit for this contact zone until this date (Bicca-Marques et al., 2008; Cortes-Ortiz et al., 2015).


Hybridization in primates is well documented for a few taxa (Cortes-Ortiz et al., 2007, 2015). As in African cercopithecines (Papio, Cercopi- thecus) (Detwiler et al., 2005), anthropogenic habitat fragmentation may increase the incidence of hybridization in howler monkeys, because the confinement of a few individuals in small fragments can reduce the chances of finding conspecific partners, which can lead to more frequent contact with groups of other species, and to interspecific crosses (Dias et al., 2013). The landscape in our study site is naturally fragmented (the municipality of Sao Vicente do Sul presents 527.71 [km.sup.2] of grasslands, and only 97.88 [km.sup.2] of forested habitats), and there are no records of extensive deforestation in recent times (UFRGS/EMBRAPA, 2007). This landscape configuration may increase the chances of hybridization, in part because of the risks associated with long distance dispersal that may be required to find conspecifics (see the case of Cercopithecus cephus and Cercopithecus nictitans in the Lope Reserve, Gabon; Detwiler et al., 2005). In our study site the narrow strips of riparian forest that remain may hamper howlers' displacements.

The study site is located exclusively within the Pampa biome, which is tipically inhabited by A. caray a (Fig. 5), but the headwaters of the Ibicui River are located in areas of seasonal deciduous forest (Atlantic Forest sensu lato) on the southern foothills of the geological formation known as Serra Geral (Leite and Klein, 1990), typically inhabited by A. guariba clamitans (Fig. 5). Thus, A. guariba clamitans may be using the riparian forest of the Ibicui River and tributaries as a dispersal route from the seasonal forest toward areas of the Pampa. As in other contact zones of A. caraya and A. guariba clamitans, the presence of both howler species in our study site is compatible with a secondary contact (Cortes-Ortiz et al., 2015), promoted by the recent expansion of gallery forests in this area (BiccaMarques et al., 2008).



The sizes of the groups recorded in our study site were smaller than in nearby areas. The monospecific group of A. caraya had only three individuals, smaller than the three groups (with 5, 10, and 15 individuals) recorded by BiccaMarques et al. (2008) in Sao Francisco de Assis (30 km to the northwest), and groups of A. guariba clamitans had only 4 or 5 individuals versus the average 5.8 ([+ or -] 2.2) in Santa Maria (90 km to the east; Fortes, 2008) and 7 individuals in a single group observed in Sao Francisco de Assis (Bicca-Marques et al., 2008). Heterospecific groups in this study were slightly larger than the average group size for A. guariba clamitans (6.9 [+ or -] 2.0 individuals, n = 3 groups in 17 study sites; Fortes et al., 2015), but smaller than the average size for A. caraya groups (9.8 [+ or -] 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 typically have a single male (Bicca-Marques et al., 2008; Fortes, 2008). The size and composition 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 distribution (Brown et al., 1995; Thomas and Kunin, 1999). Thus, heterospecific groups could be formed as result of the Allee effect--low abundance or unbalanced sex ratios lead to a difficulty to find conspecific sexual partners (Courchamp et al., 1999; Stephens and Sutherland, 1999). This could be the case in El Pinalito Provincial Park, Misiones, Argentina, where A. caraya individuals seem to be spreading into areas typically inhabited by A. guariba, or at Sao Francisco de Assis, Rio Grande do Sul, Brazil, where A. guariba clamitans groups decrease westwards, whereas the opposite trend occurs for A. caraya groups (Cortes-Ortiz et al., 2015). However, confirmation of this hypothesis requires additional data on the density of both species in this and other areas.

The coloration patterns of putative hybrid individuals indicate that there may be both male and female hybrids in this area, as recorded in the upper Parana River, Brazil (Aguiar et al., 2008), but genetic studies are needed to confirm and further characterize suspected hybridization. Additionally, demographic and behavioral studies in this area are also desirable, aimed at a more comprehensive analysis of the mechanisms that promote or maintain hybridization in howler monkeys.

Recibido 2 noviembre 2014. Aceptado 22 mayo 2015. Editor asociado: M Kowalewski


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Thomas D. Dias (1), Martha S. Conceicao (1), Laurete Murer (2), and Vanessa B. Fortes (3

(1) Laboratorio de Primatologia, Universidade Federal de Santa Maria

(2) Programa de Pos-Graduacao em Medicina Veterinaria, Centro de Ciencias Rurais, Universidade Federal de Santa Maria. Camobi, Santa Maria, RS, Brasil

(3) Laboratorio de Primatologia, Centro de Educacao Superior Norte do Rio Grande do Sul, Universidade Federal de Santa Maria, Av. Independencia 3751, Bairro Vista Alegre, Palmeira das Missoes, RS, Brasil, CEP 98.300-000. [Correspondence: Vanessa B. Fortes <>]
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 of         Coordinates         ADM      SADM

A.caraya      March 2011    29[degrees]46'04"S;      1
A. guariba    June 2012     29[degrees]46'04"S;      1
A. guariba   October 2013   29[degrees]49'38"S;      1
Mixed         July 2012     29[degrees]46'04"S;   1Ac, 1Ag   1Hy
Mixed        October 2013   29[degrees]46'07"S;     1Ac      1Hy

                  ADF        JUV    INF    NI   Group Size

A.caraya           1                 1              3

A. guariba         2          1                     4

A. guariba         2                 1     1        5

Mixed          2Ac, 1Ag      1Ac?   1Ac?            8

Mixed        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.
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Author:Dias, Thomas D.; Conceicao, Martha S.; Murer, Laurete; Fortes, Vanessa B.
Publication:Mastozoologia Neotropical
Date:Dec 1, 2015
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