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Wild mixed groups of howler species (Alouatta caraya and Alouatta clamitans) and new evidence for their hybridization

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Abstract

Mixed species groups and hybridization are common among primates, yet these phenomena are rare and poorly understood for the genus Alouatta. In this study, we describe the composition of howler groups in a sympatric area of Alouatta caraya and Alouatta clamitans and provide new evidence for the occurrence of interspecific hybridization. Between October 2006 and April 2007, 11 howler groups were located in a 150-ha forest fragment: two monospecific groups of A. caraya, two monospecific groups of A. clamitans, two groups composed of A. clamitans and hybrid morphotypes (A. caraya × A. clamitans), and five groups composed of both species together with hybrid morphotypes (mixed species groups). The average size of the studied groups was 5.2 ± 1.2 individuals. Monospecific and mixed groups (mixed species groups + groups with hybrids) did not differ significantly in their sizes. In total, the sex/age ratios were 1 AM:1.5 AF:0.2 SAM:0.5 JUV:0.2 INF and the species ratios were 1 A. caraya:1.6 A. clamitans:0.4 A. caraya × A. clamitans. The ratio of immatures to 1AF was larger in the monospecific groups (0.75 immatures:1AF) than in mixed groups (0.29 immatures:1AF), possibly reflecting a lower viability in the latter. Two features of the hybrid morphotypes of the upper Paraná River support their status as true hybrids: the polymorphism of their coloration patterns and the extremely female-biased sex ratio. The effects of Haldane’s rule and population fragmentation on the interactions between both species are discussed.

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References

  • Ackermann RR, Rogers J, Cheverud JM (2006) Identifying the morphological signatures of hybridization in primate and human evolution. J Hum Evol 51:632–645

    Article  PubMed  Google Scholar 

  • Aguiar LM, Mellek DM, Abreu KC, Boscarato TG, Bernardi IP, Miranda JMD, Passos FC (2007) Sympatry of Alouatta caraya and Alouatta clamitans and the rediscovery of free-ranging potential hybrids in Southern Brazil. Primates 48:245–248

    Article  PubMed  Google Scholar 

  • Arnold ML, Meyer A (2006) Natural hybridization in primates: one evolutionary mechanism. Zoology 109:261–276

    Article  PubMed  Google Scholar 

  • Bergman TJ, Beehner JC (2004) Social system of a hybrid baboon group (Papio anubis × P. hamadryas). Int J Primatol 25:1313–1330

    Article  Google Scholar 

  • Bynum N (2002) Morphological variation within a Macaque hybrid zone. Am J Phys Anthropol 118:45–49

    Article  PubMed  Google Scholar 

  • Campos JB (2001) Parque Nacional de Ilha Grande, re-conquista e desafios. IAP/Coripa, Maringá, Brazil

  • Cortés-Ortiz L, Bermingham E, Rico C, Rodríguez-Luna E, Sampaio I, Ruiz-García M (2000) Molecular systematics and biogeography of the neotropical monkey genus, Alouatta. Mol Phyl Evol 26:64–81

    Article  Google Scholar 

  • Cortés-Ortiz EB, Canales-Espinosa D, García-Orduña F, Rodríguez-Luna E (2006) Natural Hybridization between howler monkeys in México. Am J Primatol 68:136

    Google Scholar 

  • Detwiler KM, Burrell AS, Jolly CJ (2005) Conservation implications of hybridization in African cercopithecine monkeys. Int J Primatol 26:661–684

    Article  Google Scholar 

  • Di Bitetti MS, Placci G, Brown AD, Rode DI (1994) Conservation and population status of the brown howling monkey (Alouatta fusca clamitans) in Argentina. Neotrop Primates 2:1–4

    Google Scholar 

  • Gregorin R (2006) Taxonomia e variação geográfica das espécies do gênero Alouatta Lacépède (Primates, Atelidae) no Brasil. Rev Bras Zool 23:64–144

    Article  Google Scholar 

  • Mendes SL (1997) Hybridization in free-ranging Callithrix flaviceps and the taxonomy of the Atlantic Forest marmosets. Neotrop Primates 5:6–8

    Google Scholar 

  • Miranda JMD, Passos FC (2005) Composição e dinâmica de grupos de Alouatta guariba clamitans Cabrera (Primates, Atelidae) em Floresta Ombrófila Mista no Estado do Paraná, Brasil. Rev Bras Zool 22:99–106

    Google Scholar 

  • Mudri MD, Rahn M, Gorostiaga M, Hick A, Merani MS, Solari AJ (1998) Revised karyotype of Alouatta caraya (Primates: Platyrrhini) based on synaptonemal complex and banding analyses. Hereditas 128:9–16

    Article  Google Scholar 

  • Peres CA, Patton JL, Da Silva MNF (1996) Riverine barriers and gene flow in Amazonian saddle-back tamarin monkeys. Folia Primatol 67:113–124

    PubMed  CAS  Google Scholar 

  • Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109

    Article  Google Scholar 

  • Rumiz DI (1990) Alouatta caraya: population density and demography in Northern Argentina. Am J Primatol 21:279–294

    Article  Google Scholar 

  • Silva BTF, Sampaio MIC, Schneider H, Schineider MPC, Montoya E, Encarnación F, Salzano FM (1992) Natural hybridization between Saimiri Taxa in the Peruvian Amazônia. Primates 33:107–113

    Article  Google Scholar 

  • Stensland E, Angerbjörn A, Berggren P (2003) Mixed species groups in mammals. Mammal Rev 33:205–223

    Article  Google Scholar 

  • Terborgh J (1990) Mixed flocks and polyspecific associations: costs and benefits of mixed groups to birds and monkeys. Am J Primatol 21:87–100

    Article  Google Scholar 

  • Wu C, Johnson NA, Palopoli MF (1996) Haldane’s rule and its legacy: why are there so many sterile males? Tree 11:281–284

    Google Scholar 

Download references

Acknowledgments

We thank CNPq for a scholarship to LM Aguiar and for a research grant to FC Passos, APA Municipal de Alto Paraíso, Ilha Grande National Park, nine research assistants for help during field work, IBAMA for permit 261/2006, and two anonymous reviewers for helpful suggestions about the manuscript. JMD Miranda provided valuable statistical advice.

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Authors and Affiliations

  1. Programa de Pós-graduação em Zoologia, UFPR, Laboratório de Biodiversidade, Conservação e Ecologia de Animais Silvestres, Departamento de Zoologia, Universidade Federal do Paraná, Caixa Postal 19020, 81531-990, Curitiba, Paraná, Brazil

    Lucas M. Aguiar & Fernando C. Passos

  2. Laboratório de Ecologia Molecular e Parasitologia Evolutiva, Departamento de Zoologia, UFPR, Curitiba, Paraná, Brazil

    Marcio R. Pie

Authors
  1. Lucas M. Aguiar
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  2. Marcio R. Pie
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  3. Fernando C. Passos
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Corresponding author

Correspondence to Lucas M. Aguiar.

Additional information

Contribution number 1689 of the Departamento de Zoologia, Universidade Federal do Paraná (UFPR), Caixa Postal 19020, 81531-990, Curitiba, Paraná, Brazil. Contract grant sponsor: Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

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Aguiar, L.M., Pie, M.R. & Passos, F.C. Wild mixed groups of howler species (Alouatta caraya and Alouatta clamitans) and new evidence for their hybridization. Primates 49, 149–152 (2008). https://doi.org/10.1007/s10329-007-0065-y

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  • DOI: https://doi.org/10.1007/s10329-007-0065-y

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