Abstract
Records of sympatry between Alouatta caraya and A. clamitans are rare despite their extensive range overlap. An example of their current sympatry and the rediscovery of free-ranging potential hybrids of A. caraya and A. clamitans in the forests of the Upper Paraná River, Southern Brazil, are reported in this paper. Eight groups were observed in the study area: five monospecific groups of A. caraya, two of A. clamitans, and a group containing two adult males and two adult females of A. caraya and a sub-adult male and two adult females identified as Alouatta sp. The color of the last three individuals was a mosaic between the two species; this is consistent with previously described variations in museum specimens collected in the Paraná River in the 1940s that had been identified as potential hybrids. The results from this study emphasize the need for scientific studies in the region of the Ilha Grande National Park, one of the few regions in the Paraná River that currently harbors both howler species.
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Introduction
According to Groves (2001) the genus Alouatta comprises ten recognized species. This number varies depending on taxonomic treatment, however (Rylands et al. 2000; Gregorin 2006). The genus has the broadest geographical distribution among Neotropical primates (Platyrrhini), occurring from the south of the State of Veracruz, in Mexico, to Northern Argentina and Southern Brazil (Hirsch et al. 1991; Cortés-Ortiz et al. 2003).
In general, Alouatta species are distributed in a parapatric fashion, with possible contact zones between rivers that represent the limits of their distribution. Potential contact zones of A. pigra and A. palliata have been recorded between the Grijalva and Usumacinta Rivers (Cortés-Ortiz et al. 2003), those of A. palliata and A. seniculus between the Atrato and Sinú Rivers (Defler 2004), those of A. seniculus and A. belzebul between the Santa Helena, Madeira, and Tapajós Rivers (Hirsch et al. 1991; Pinto and Setz 2000), those of A. seniculus and A. caraya between the Blanco and Guaporé Rivers (Wallace et al. 2000; Iwanaga and Ferrari 2002), those of A. belzebul and A. caraya at the head of the Parnaíba River (Chame and Olmos 1997), and those of A. caraya and A. clamitans between the Paraná and Uruguay Rivers (Hirsch et al. 1991; Di Bitetti et al. 1994; Di Bitetti 2005; Gregorin 2006).
Although the contact zone between A. caraya and A. clamitans is extensive, historical or recent records of their sympatry are rare. The first indications of sympatry were the specimens collected by A. Mayer in the forests of the Upper Paraná River in the 1940s. The capture site of A. caraya (Iguaçu National Park) is, however, approximately 300 km from the capture site of A. clamitans (a location known as the “Sertão do Rio Paraná”) (data obtained in Lorini and Persson 1990). At that time three females were collected at the “Sertão do Rio Paraná” and deposited as Alouatta sp. in the Museu de História Natural do Capão da Imbúia (MHNCI). The hair coloration of these specimens does not correspond to the patterns known for the two species that occur in the region. The hair is, however, distinctly arranged in a mosaic between the typical female colorations of A. caraya and A. clamitans, and cannot, therefore, be regarded as distinct from those species (Gregorin 2006). Systematic studies of these specimens emphasized the possibility they were hybrids of these species in that site (Lorini and Persson 1990; Gregorin 2006).
The most recent recorded case of sympatry was published by Di Bitetti (2005), who reported the existence of both species in the Provincial Piñalito Park, between the Paraná and Uruguay Rivers in Argentina. Recent efforts, however (Aguiar 2006; Aguiar et al. 2007), did not find these species coexisting in the region of the Upper Paraná River.
In December of 2005 our team collected a specimen of A. clamitans that had been run over on the BR-487 highway, next to the border between the States of Paraná and Mato Grosso do Sul, in the immediate surroundings of the Ilha Grande National Park. We then organized an expedition to search for both howler species in this park. In this paper we report the current existence of sympatry and the rediscovery of morphotypes with intermediate coloration which are possible free-ranging hybrids between A. caraya and A. clamitans.
Materials and methods
Study area
The sampled area included a 17-km stretch of riparian forest and an adjacent forest fragment (“Mata do Bugio” 150 ha) (Fig. 1). This region belongs to the left margin of the Paraná River, from Porto Figueira (municipality of Alto Paraíso) to 4 km upstream of Porto Camargo (Municipality of Icaraíma), State of Paraná, Southern Brazil. The region is located in the Federal Area for Environmental Protection (APA) of the Islands and Flood Plains of the Paraná River, in the immediate surroundings of the Ilha Grande National Park (23°15′ to 24°05′S and 53°40′ to 54°17′W), in the flood plains of the Upper Paraná River. Average annual temperature is 22°C, with 1,200 to 1,300 mm of rainfall and a Cfa climate according Köeppen’s classification (Campos 2001). The forests in the region are flooded periodically and are classified as seasonal semideciduous alluvial forest. This vegetation is characterized by low arboreal diversity, with Cecropia pachystachya the dominant species in riparian forests (Souza et al. 2004). Some authors regard this region as an ecotone between the Atlantic Rainforest and the Cerrado (Campos 2001; Souza et al. 2004).
Methods
Field efforts to search for the primates in the study site occurred in April 2006, with separate incursions into the riparian and mainland forests. The former was searched for 2 days using a boat that went upstream for 17 km starting in Porto Figueira, followed by a 17 km return using hiking trails. The mainland forest was searched during 1 day by means of a 3 km walk outside the hiking trails. Primates were located by use of binoculars.
Results
Three primate species were detected and identified as forming monospecific groups on the riparian forests—five groups of A. caraya, two groups of A. clamitans, and a group of Cebus nigritus. In a site known as “Paredão das Araras” (23°21′10.1″S and 53°44′08.5″W) there was a record of a group of A. caraya living about 30 m from a group of A. clamitans.
In the “Mata do Bugio” (23°22′52.3″S and 053°45′39.6″W) a group of seven Alouatta individuals was found and followed. This group comprised two adult males and two adult females of A. caraya, and a sub-adult male and two adult females identified a priori as Alouatta sp.. These individuals had a mosaic coloration pattern—the front, head, face and legs were dark brown (characteristic of A. clamitans), yet the tail, hands and feet were pale yellowish-brown (characteristic of A. caraya). The coloration pattern of the sub-adult male is shown in Fig. 2. At first, all the animals in this group were resting in the same tree. Later, two females of Alouatta sp. were observed grooming a single adult male of A. caraya while a female of A. caraya and a sub-adult male of Alouatta sp. fed on leaves of the tree where they were located.
Discussion
The sympatry observed in this study indicates that this region of the Paraná River can be regarded as a zone of faunistic contact, reflecting the vegetational limits of the Cerrado and the Atlantic Rainforest. Alouatta caraya is a howler that is characteristic of Central Brazil, occurring mostly within the limits of the Cerrado (Wallace et al. 2000; Gregorin 2006), whereas A. clamitans is characteristic of the south and southeast of the Atlantic Rainforest (Gregorin 2006).
The occurrence of sympatry among congeneric Neotropical primates is thought to be rare, because of the similarity of their niches, particularly in comparison with Old World primates (Peres and Janson 1999; Ferrari 2004). Habitat destruction might cause sympatry to be even more uncommon because of competition between sympatric species. Some authors have pointed out that the absence of A. clamitans in other regions of the Paraná River might be because of severe anthropogenic disturbance of those environments (Di Bitetti et al. 1994; Codenotti et al. 2002; Di Bitetti 2005; Aguiar 2006). In contrast, the same authors asserted that A. caraya is more tolerant of the effects of forest fragmentation and is still found in those habitats. The sympatry of both howler species in the region of the Ilha Grande National Park seems, therefore, to indicate the existence of a relatively preserved area where both species can coexist. In contrast with observations by Di Bitetti (2005) in Argentina, the sympatry region in our study is located on the left margin of the Paraná River. In Argentina, Di Bitetti recorded this range overlap in the region between the Paraná and Uruguay Rivers, and suggested that A. caraya was replacing A. clamitans near the margins of the Paraná River because of anthropic effects on the forest.
The animals identified in this study as Alouatta sp. are probably hybrids between A. caraya and A. clamitans. Their pattern is the same as that observed for the female MHNCI.031 that was captured in the “Sertão do Rio Paraná” in 1945. With two other females, that specimen was identified by Lorini and Persson (1990) and Gregorin (2006) as a possible hybrid between the species. The possibility these animals with aberrant color pattern represent natural variations or other processes, for example inbreeding or genetic drift cannot yet be excluded, however. Irrespective of the real cause, this study confirms the current existence of these animals in nature, and that this particular coloration pattern can also occur in males (previous specimens were all females).
The behavior of the animals in the group of the Mata do Bugio (e.g. rest, feeding, and grooming simultaneously in a single tree) corroborate the notion that the individuals form a cohesive group. Although Cortés-Ortiz et al. (2003) reported the existence of mixed groups between the sister species A. palliata and A. pigra, the group with possible hybrids observed in this study is of particular interest for two reasons. First, the striking difference in coloration between the species does not seem to be a reproductive barrier. Alouatta caraya and A. clamitans are sexually dimorphic in their coloration as adults. In general, adult males of A. caraya are black, and adult females are pale yellowish-brown, whereas males of A. clamitans are red and its females are dark brown. These characteristics have been thought to result from sexual selection (Bicca-Marques and Calegaro-Marques 1998; Hirano 2003), serving as mate choice signals and as prezygotic isolation mechanisms. If the existence of hybridization is corroborated, the different coloration of the species is not the only relevant factor, nor the only interspecific reproductive barrier. Second, the divergence between these species (5.1 Ma, Cortés-Ortiz et al. 2003) is not sufficient for evolution of pre-zygotic reproductive isolation between them. The species are not closely related—A. caraya being more closely related to Amazon species whereas A. clamitans is more closely related to another Atlantic Rainforest species, A. belzebul (Cortés-Ortiz et al. 2003).
The Ilha Grande National Park and its surrounding areas are among the few regions that still harbor both howler species, and thus deserve more intense scientific investigation. Genetic, behavioral, and ecological studies will be instrumental in assessing the fitness of these morphotypes and revealing the nature of such variations.
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Acknowledgments
We thank Marcelo Brunning, Rodrigo F. Moro-Rios, Gabriela Ludwig, Eduardo Carrano, Marcio R. Pie, APA das Ilhas e Várzeas do Rio Paraná, APA Municipal de Alto Paraíso, Parque Nacional de Ilha Grande, Universidade Federal do Paraná, Conselho Nacional de Pesquisa e Desenvolvimento Tecnológico (CNPq). Dr Jean P. Boubli and two other reviewers provided helpful comments on the manuscript. Contract grant sponsor: Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).
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Contribution number 1637 of the Departamento de Zoologia, Universidade Federal do Paraná, Caixa Postal 19020, 81531-980, Curitiba, Paraná, Brasil.
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Aguiar, L.M., Mellek, D.M., Abreu, K.C. et al. Sympatry between Alouatta caraya and Alouatta clamitans and the rediscovery of free-ranging potential hybrids in Southern Brazil. Primates 48, 245–248 (2007). https://doi.org/10.1007/s10329-007-0039-0
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DOI: https://doi.org/10.1007/s10329-007-0039-0