International Journal of Primatology

, Volume 36, Issue 6, pp 1198–1215 | Cite as

Do Habitat Use and Interspecific Association Reflect Predation Risk for the Golden-Headed Lion Tamarin (Leontopithecus chrysomelas)?

  • Juliana Monteiro de Almeida Rocha
  • Kristel Myriam De Vleeschouwer
  • Paula Pedreira Reis
  • Carlos Eduardo de V. Grelle
  • Leonardo C. Oliveira


Predation risk may affect the way species use their habitat. Interspecific associations can help to improve predator detection and avoidance. The golden-headed lion tamarin (Leontopithecus chrysomelas) is an endangered primate of the Brazilian Atlantic Forest whose geographical range is dominated by shaded cacao agroforest (cabruca), where predation risk is high and mainly due to raptors. We investigated whether predation risk affects vertical stratum use and time spent traveling by tamarins, and the role of interspecific association with Wied’s marmosets (Callithrix kuhlii) in shaping these activities. We compared the behavior of three tamarin groups in cabruca (March 2010–June 2011) with that of three groups in mosaic forests (January 2007–December 2008), where predation risk is lower. We predicted that tamarins would use the higher strata level less in cabruca than in mosaic forests, and would use it less after encounters with predators than before such encounters. We also predicted increased use of the higher level and increased travel during interspecific associations than when tamarins were alone. We found that tamarins avoided the higher level regardless of habitat, but used it more often in cabruca than in mosaic forest, and did not avoid it after encounters with predators. Interspecific associations did not influence tamarins’ activities, except for the smallest group of tamarins in mosaic forest, which decreased its use of the lower level when in an interspecific association. Our results suggest that the benefits of interspecies association are not related to the activities investigated here, and that predation risk can influence habitat use but vegetation structure may constrain its optimal use by primates, increasing their vulnerability to predation.


Agroforest Antipredator behavior Callithrichidae Mixed group Platyrrhini Primates 



We are grateful to the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA), Instituto Chico Mendes de Biodiversidade (ICMBio), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the permissions to conduct this study. We thank the owners and employees of the farms Almada, Santa Rita, and Bomfim for support and permission to work on their properties; the reserve directors Saturnino Sousa and Paulo Cruz for permission and support during the field activities of Project Bio Brasil in the Una Biological Reserve; the field assistants Jiomário dos Santos Souza, Josinei da Silva Santos, Antônio Ribeiro Santos Jr., José Alves das Neves Filho, and Roque da Silva Santos for help in data collection; and the Centre for Research and Conservation of the Royal Zoological Society of Antwerp (CRC-RZSA) and the Instituto de Estudos Socioambientais do Sul da Bahia (IESB) for administrative and logistic support. This manuscript was improved by the comments of Joanna M. Setchell, Paul Garber, and four anonymous reviewers. We also thank Gustavo Carvalho for help with the statistical analysis. Financial support for the Project Cabruca was provided by Lion Tamarins of Brazil Fund, Rufford Small Grants Foundation, and Centre for Research and Conservation/Royal Zoological Society of Antwerp. Financial support for the Project BioBrasil was provided by the National Lottery of Belgium, the Flemish Ministry of Science (Belgium), the Lion GHLTs of Brazil Fund, Primate Action Fund/Conservation International, and the Zoological Society of London. We also thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) for student fellowships.


  1. Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour, 49(3–4), 227–267.PubMedCrossRefGoogle Scholar
  2. Animal Behavior Society. (2012). Guidelines for the treatment of animals in behavioural research and teaching. Animal Behaviour, 83, 301–309.CrossRefGoogle Scholar
  3. Boinski, S., Treves, A., & Chapman, C. A. (2000). A critical evaluation of the influence of predators on primates: Effects on group travel. In S. Boinski & P. A. Garber (Eds.), On the move: How and why animals travel in groups (pp. 43–72). Chicago: University of Chicago Press.Google Scholar
  4. Bshary, R., & Noë, R. (1997a). Anti-predation behaviour of red colobus monkeys in the presence of chimpanzees. Behavioural Ecology and Sociobiology, 41, 321–333.CrossRefGoogle Scholar
  5. Bshary, R., & Noë, R. (1997b). Red colobus and diana monkeys provide protection against predators. Animal Behaviour, 54, 1461–1474.PubMedCrossRefGoogle Scholar
  6. Buchanan-Smith, H. M., & Hardie, S. M. (1997). Tamarin mixed-species group: an evaluation of a combined captive and field approach. Folia Primatologica, 68, 272–286.CrossRefGoogle Scholar
  7. Chapman, C. A., & Chapman, L. J. (2000). Interdemic variation in mixed-species association patterns: common diurnal primates of Kibale National Park, Uganda. Behavioural Ecology and Sociobiology, 47, 129–139.CrossRefGoogle Scholar
  8. Cheney, D. L., & Wrangham, R. W. (1987). Predation. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 227–239). Chicago: University of Chicago Press.Google Scholar
  9. Cheney, D. L., Seyfarth, R. M., Fischer, J., Beehner, J., Bergman, T., Johnson, S. E., Kitchen, D. M., Palombit, R. A., Rendall, D., & Silk, J. B. (2004). Factors affecting reproduction and mortality among baboons in the Okavango Delta, Botswana. International Journal of Primatology, 25(2), 401–428.CrossRefGoogle Scholar
  10. Curio, E. (1976). The ethology of predation. Berlin: Springer-Verlag.CrossRefGoogle Scholar
  11. Curio, E. (1978). The adaptive significance of avian mobbing. I. Teleonomic hypotheses and predictions. Zeitschrift für Tierpsychologie, 48, 175–183.Google Scholar
  12. Dacier, A., Maia, R., Agustinho, D. P., & Barros, M. (2006). Rapid habituation of scan behavior in captive marmosets following brief predator encounters. Behavioural Processes, 71, 66–69.PubMedCrossRefGoogle Scholar
  13. Day, R. T., & Elwood, R. W. (1999). Sleeping site selection by the golden-handed tamarin Saguinus midas midas: the role of predation risk, proximity to feeding sites, and territorial defence. Ethology, 105, 1035–1051.CrossRefGoogle Scholar
  14. Dietz, J., de Sousa, S., & Billerbeck, R. (1996). Population dynamics of golden-headed lion GHLTs in Una Reserve, Brazil. Dodo Journal of Wildlife Preservation Trusts, 32, 115–122.Google Scholar
  15. Ferrari, F. S. (2009). South American primates: Comparative perspectives in the study of behavior, ecology and conservation. In P. A. Garber, A. Estrada, J. C. Bicca-Marques, E. W. Heymann, & K. B. Strier (Eds.), Developments in Primatology: Progress and prospects (pp. 251–277). New York: Springer Science+Business Media.Google Scholar
  16. Fleagle, J. G. (1988). Primate Adaptation and Evolution. San Diego: Academic Press, p. 596.Google Scholar
  17. Galleti, M., & Sazima, I. (2006). Impacto de cães ferais em um fragmento urbano de Floresta Atlântica no sudeste do Brasil. Natureza & Conservação, 4(1), 58–63.Google Scholar
  18. Garber, P. A. (1988). Diet, foraging patterns, and resource defense in a mixed species troop of Saguinus mystax and Saguinus fuscicollis in Amazonian Peru. Behaviour, 105, 18–34.CrossRefGoogle Scholar
  19. Garber, P. A., & Bicca-Marques, J. C. (2002). Evidence of predator sensitive foraging and traveling in single-and mixed-species tamarin troops. In L. E. Miller (Ed.), Eat or be eaten: Predator sensitive foraging among primates (pp. 138–153). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  20. Gautier-Hion, A., Quris, R., & Gautier, J. (1983). Monospecific versus polyspecific life: a comparative study of foraging and antipredatory tactics in a community of Cercopithecus monkeys. Behavioral Ecology and Sociobiology, 12, 325–335.CrossRefGoogle Scholar
  21. Gouvêa, J. B. S., Silva, L. A. M., & Hori, M. (1976). Fitogeografia. In Comissão Executiva do Plano da Lavoura Cacaueira e Instituto Interamericano de Ciências Agrícolas (Ed.), Diagnóstico sócio econômico da região cacaueira (pp. 1–10). Ilhéus: CEPLAC.Google Scholar
  22. Gursky, S., & Nekaris, K. A. I. (2007). Primate anti-predator strategies. New York: Springer Science+Business Media.CrossRefGoogle Scholar
  23. Hamilton, W. D. (1971). Geometry for the selfish herd. Journal of Theoretical Biology, 31(2), 295–311.PubMedCrossRefGoogle Scholar
  24. Hankerson, S. J., & Caine, N. G. (2004). Pre-retirement predator encounters alter the morning behavior of captive marmosets (Callithrix geoffroyi). American Journal of Primatology, 63, 75–85.PubMedCrossRefGoogle Scholar
  25. Hart, D. (2007). Predation on primates: A biogeographical analysis. In S. Gursky & K. A. I. Nekaris (Eds.), Primate anti-predator strategies (pp. 27–59). New York: Springer Science+Business Media.CrossRefGoogle Scholar
  26. Heymann, E. W. (1990). Reactions of wild tamarins, Saguinus mystax and Saguinus fuscicollis to avian predators. International Journal of Primatology, 11(4), 327–337.CrossRefGoogle Scholar
  27. Heymann, E. W., & Buchanan-Smith, H. M. (2000). The behavioural ecology of mixed-species troops of callitrichine primates. Biological Reviews, 75, 169–190.PubMedCrossRefGoogle Scholar
  28. Hill, R. A., & Dunbar, R. I. M. (1998). An evaluation of the roles of predation risk as selective pressure on primate grouping behaviour. Behaviour, 135, 411–430.CrossRefGoogle Scholar
  29. IUCN (2015). IUCN Red List of threatened species, version 2015.1. Accessed 17 Aug 2015.
  30. Izawa, K. (1978). A field study of the ecology and behavior of the black-mantle tamarin (Saguinus nigricollis). Primates, 19, 241–274.CrossRefGoogle Scholar
  31. Johns, N. D. (1999). Conservation in Brazil’s chocolate forest: the unlikely persistence of the traditional cocoa agroecosystem. Environmental Management, 23(1), 31–47.PubMedCrossRefGoogle Scholar
  32. Lima, S. L., & Dill, L. (1990). Behavioural decisions made under risk of predation: a review and prospectus. Canadian Journal of Zoology, 68, 619–640.CrossRefGoogle Scholar
  33. Lucas, J. R., Waser, M. P., & Creel, S. R. (1994). Death and disappearance: estimating mortality risks associated with philopatry and dispersal. Behavioral Ecology, 5(2), 135–141.CrossRefGoogle Scholar
  34. Madden, D., Garber, P. A., Madden, S. L., & Snyder, C. A. (2010). Rain-forest canopy-connectivity and habitat selection by a small neotropical primate, Geoffroy’s tamarin (Saguinus geoffroyi). Journal of Tropical Ecology, 26(6), 637–644.CrossRefGoogle Scholar
  35. McGraw, W. S., & Bshary, R. (2002). Association of terrestrial mangabeys (Cercocebus atys) with arboreal monkeys: experimental evidence for the effects of reduced ground predator pressure on habitat use. International Journal of Primatology, 23(2), 311–325.CrossRefGoogle Scholar
  36. McNamara, J. M., & Houston, A. I. (1987). Starvation and predation as factors limiting population size. Ecology, 68(5), 1515–1519.CrossRefGoogle Scholar
  37. Miranda, J. M. D., Itiberê, P. D., Bernardi, P., Moro-Rios, R. F., & Passos, F. C. (2006). Antipredator behavior of brown howlers attacked by black hawk-eagle in southern Brazil. International Journal of Primatology, 27(4), 1907–1101.CrossRefGoogle Scholar
  38. Mori, S. A., Boom, B. M., Carvalho, A. M., & Santos, T. S. (1983). Southern Bahian moist forests. Botanical Review, 49, 155–232.CrossRefGoogle Scholar
  39. Oliveira, L. C., & Dietz, J. M. (2011). Predation risk and the interspecific association of two Brazilian Atlantic Forest primates in cabruca agroforest. American Journal of Primatology, 73, 1–9.CrossRefGoogle Scholar
  40. Oliveira, V. B., Linares, A. M., Corrêa, G. L. C., & Chiarello, A. G. (2008). Predation on the black capuchin monkey Cebus nigritus (Primates: Cebidae) by domestic dogs Canis lupus familiaris (Carnivora: Canidae), in the Parque Estadual Serra do Brigadeiro, Minas Gerais, Brazil. Revista Brasileira de Zoologia, 25(2), 376–378.CrossRefGoogle Scholar
  41. Oliveira, L. C., Neves, L. G., Raboy, B. E., & Dietz, J. M. (2011). Abundance of jackfruit (Artocarpus heterophyllus) affects group characteristics and use of space by golden-headed lion GHLTs (Leontopithecus chrysomelas) in cabruca agroforest. Environmental Management, 48(2), 248–262.PubMedCrossRefGoogle Scholar
  42. Peres, C. A. (1992). Consequences of joint-territoriality in a mixed-species group of tamarin monkeys source. Behaviour, 123(3/4), 220–246.CrossRefGoogle Scholar
  43. Peres, C. A. (1993). Anti-predation benefits in a mixed-species group of Amazonian tamarins. Folia Primatologica, 61, 61–76.CrossRefGoogle Scholar
  44. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & Development Core Team, R. (2013). nlme: linear and nonlinear mixed effects models. R package version, 3, 1–111.Google Scholar
  45. Porter, L. M. (2001). Benefits of polyspecific associations for the Goeldi’s monkey (Callimico goeldii). American Journal of Primatology, 54, 143–158.PubMedCrossRefGoogle Scholar
  46. Porter, L. M., & Garber, P. A. (2007). Niche expansion of a cryptic primate, Callimico goeldii, while in mixed species troops. American Journal of Primatology, 69, 1340–1353.PubMedCrossRefGoogle Scholar
  47. R Core Team (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  48. Raboy, B. E. (2002). The ecology and behavior of wild golden headed lion tamarins (Leontopithecus chrysomelas). Dissertation, College Park (MD): University of Maryland. 161p.Google Scholar
  49. Raboy, B. E., & Dietz, J. M. (2004). Diet, foraging, and use of space in wild golden-headed lion tamarins. American Journal of Primatology, 63, 1–15.PubMedCrossRefGoogle Scholar
  50. Raboy, B. E., Neves, L. G., Zeigler, S. L., Saraiva, N., Cardoso, N., Santos, G., Ballou, J., & Leimgruber, P. (2010). Strength of habitat and landscape metrics in predicting golden-headed lion tamarin presence or absence in forest patches. Biotropica, 42(3), 388–397.CrossRefGoogle Scholar
  51. Rylands, A. B. (1989). Sympatric Brazilian callithrichids: the black tufted-ear marmoset, Callithrix kuhli, and the golden-headed lion tamarin, Leontopithecus chrysomelas. Journal of Human Evolution, 18, 679–695.CrossRefGoogle Scholar
  52. Rylands, A. B. (1993). The ecology of the lion GHLTs, Leontopithecus: Some intrageneric differences and comparisons with other callitrichids. In A. B. Rylands (Ed.), Marmosets and GHLTs: Systematics, behaviour, and ecology (pp. 296–313). Oxford: Oxford University Press.Google Scholar
  53. Sambuichi, R. H. R. (2002). Fitossociologia e diversidade de espécies arbóreas em cabruca (mata atlântica raleada sobre plantação de cacau) na região sul da Bahia, Brasil. Acta Botânica Brasílica, 16, 89–101.CrossRefGoogle Scholar
  54. Sambuichi, R. H. R. (2006). Estrutura e dinâmica do componente arbóreo em área de cabruca na região cacaueira do sul da Bahia, Brasil. Acta Botânica Brasílica, 20(4), 943–954.CrossRefGoogle Scholar
  55. Smith, A. C., Kelez, S., & Buchanan-Smith, H. M. (2004). Factors affecting vigilance within wild mixed-species troops of saddleback (Saguinus fuscicollis) and moustached GHLTs (S. mystax). Behavioral Ecology and Sociobiology, 56, 18–25.CrossRefGoogle Scholar
  56. Stanford, C. B. (2002). Avoiding predators: expectations and evidence in primate antipredator behavior. International Journal of Primatology, 23(4), 741–757.CrossRefGoogle Scholar
  57. Stojan-Dolar, M., & Heymann, E. W. (2010). Vigilance of mustached tamarins in single-species and mixed-species groups – the influence of group composition. Behavioural Ecology and Sociobiology, 64, 325–335.CrossRefGoogle Scholar
  58. Sussman, R. W., & Kinzey, W. G. (1984). The ecological role of the Callitrichidae: a review. American Journal of Physical Anthropology, 64, 419–449.PubMedCrossRefGoogle Scholar
  59. Terborgh, J. (1983). Five new world primates. Princeton: Princeton University Press.Google Scholar
  60. Terborgh, J. (1986). The social systems of New World primates: An adaptationist view. In J. G. Else & P. C. Lee (Eds.), Primate ecology and conservation (pp. 199–211). Cambridge: Cambridge University Press.Google Scholar
  61. Terborgh, J. (1990). Mixed flocks and polyspecific associations: costs and benefits of mixed-groups to birds and monkeys. American Journal of Primatology, 21, 87–100.CrossRefGoogle Scholar
  62. van Schaik, C. P., van Noordwijk, M. A., Warsono, B., & Sutriono, E. (1983). Party size and early detection of predators in Sumatran forest primates. Primates, 24, 211–221.CrossRefGoogle Scholar
  63. Vanak, A. T., & Gompper, M. E. (2009). Dogs Canis familiaris as carnivores: their role and function in intraguild competition. Mammal Review, 39, 265–283.CrossRefGoogle Scholar
  64. Zeigler, S. L., Fagan, W. F., DeFries, R., & Raboy, B. E. (2010). Identifying important forest patches for the long-term persistence of the endangered golden-headed lion tamarin (Leontopithecus chrysomelas). Tropical Conservation Science, 3(1), 63–77.Google Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Juliana Monteiro de Almeida Rocha
    • 1
    • 2
  • Kristel Myriam De Vleeschouwer
    • 2
    • 3
  • Paula Pedreira Reis
    • 2
    • 4
  • Carlos Eduardo de V. Grelle
    • 1
  • Leonardo C. Oliveira
    • 1
    • 4
    • 5
    • 6
  1. 1.Programa de Pós-Graduação em EcologiaUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  2. 2.Instituto de Estudos Socioambientais do Sul da Bahia (IESB)IlhéusBrazil
  3. 3.Centre for Research and ConservationRoyal Zoological Society of AntwerpAntwerpBelgium
  4. 4.Programa de Pós-Graduação em Ecologia e Conservação da BiodiversidadeUniversidade Estadual de Santa CruzIlhéusBrazil
  5. 5.Bicho do Mato Instituto de PesquisasBelo HorizonteBrazil
  6. 6.Faculdade de Formação dos ProfessoresUniversidade do Estado do Rio de Janeiro (FFP/UERJ)São GonçaloBrazil

Personalised recommendations