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A green racer snake (Philodryas nattereri, Colubridae) killed but not eaten by a blonde capuchin monkey (Sapajus flavius, Cebidae)

Abstract

We report the killing of a snake (Philodryas nattereri, Colubridae) by a blonde capuchin monkey (Sapajus flavius, Cebidae). This endemic primate species from the northeast of Brazil includes vertebrates such as lizards and marsupials in its diet, but we can find no previously published record of an attack upon or consumption of snakes by this species of platyrhine monkey. During the attack, the group mobbed the snake, with individuals uttering agonistic vocalizations and displaying behaviors such as raising their tails, moving tree branches, piloerecting, and baring their teeth. An adult male monkey seized the snake, bit and twisted its body, thereby killing it; he then dropped the carcass onto tree branches, but did not consume it. This single event suggests that this Cebidae species may be able to distinguish dangerous from harmless snakes, and it also may be an example of a lethally violent reaction to a potential predator or competitor, exemplifying the plasticity and cognitive skills exhibited by genus Sapajus.

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Fig. 1

Source: Gibran Anderson

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Source: Gibran Anderson

Fig. 3

Source: Gibran Anderson

References

  1. Bacalhao MBM, Firmino MO, Siqueira RAS et al (2016) Morphological description of two species of Sapajus found in Paraíba: S. libidinosus and the newly discovered and endangered S. flavius. Pesqui Vet Bras 36:317–321. https://doi.org/10.1590/S0100-736X2016000400011

    Article  Google Scholar 

  2. Blumenschine RJ, Cavallo JA (1992) Scavenging and human evolution. Sci Am 267:90–96. https://doi.org/10.1038/scientificamerican1092-90

    Article  CAS  PubMed  Google Scholar 

  3. Boinski S (1988) Use of a club by a wild white faced capuchin (Cebus capucinus) to attack a venomous snake (Bothrops asper). Am J Primatol 14:177–179. https://doi.org/10.1002/ajp.1350140208

    Article  Google Scholar 

  4. Boitani L, Fragaszy DM, Boinski S (1995) Patterns of individual diet choice and efficiency of foraging in wedge-capped capuchin monkeys (Cebus olivaceus). J Comp Psychol 109:339. https://doi.org/10.1037/0735-7036.109.4.339

    Article  Google Scholar 

  5. Chapman CA (1986) Boa constrictor predation and group response in white-faced cebus monkeys. Biotropica 18:171–172. https://doi.org/10.2307/2388761

    Article  Google Scholar 

  6. da Silva GAO, Freitas NDA, de L Marinho PE et al (2018) Efeitos da presença humana sobre as interações sociais de macacos-pregos-galegos (Sapajus flavius) em cativeiro. Rev Nord Biol 26:84–103. https://doi.org/10.22478/ufpb.2236-1480.2018v26n1.46025

    Article  Google Scholar 

  7. de Araújo MB (2013) Comunicação vocal em Sapajus flavius na natureza. Universidade Federal de Pernambuco. Pernambuco: University Federal of Pernambuco Press. https://repositorio.ufpe.br/bitstream/123456789/11746/1/Disserta%C3%A7%C3%A3o%20Monique%20Bastos.pdf. Accessed 11 July 2019

  8. de Mesquita PCMD, Borges-Nojosa DM, Passos DC, Bezerra CH (2011) Ecology of Philodryas nattereri in the Brazilian semi-arid region. Herpetol J 21:193–198. https://www.thebhs.org/publications/the-herpetological-journal/volume-21-number-3-July-2011/630-06-ecology-of-i-philodryas-nattereri-i-in-the-brazilian-semi-arid-region/file. Accessed 11 July 2019

  9. Fack V, Shanee S, Drubbel RV, et al (2018) Observation of snake (Colubridae) predation by yellow-tailed woolly monkeys (Lagothrix flavicauda) at el Toro study site, Peru. Neotrop Primates 24:79–82. http://static1.1.sqspcdn.com/static/f/1200343/28089189/1551555846163/NP24.2.pdf?token=FbPe5kTovzqp6mq9n3SWIQTLndQ%3D. Accessed 11 July 2019

  10. Falótico T, Verderane MP, Mendonça-Furtado O et al (2018) Food or threat? Wild capuchin monkeys (Sapajus libidinosus) as both predators and prey of snakes. Primates 59:99–106. https://doi.org/10.1007/s10329-017-0631-x

    Article  PubMed  Google Scholar 

  11. Ferrari SF, Beltrão-Mendes R (2011) Do snakes represent the principal predatory threat to callitrichids? Fatal attack of a viper (Bothrops leucurus) on a common marmoset (Callithrix jacchus) in the Atlantic Forest of the Brazilian northeast. Primates 52(3):207–209. https://doi.org/10.1007/s10329-011-0260-8

    Article  PubMed  Google Scholar 

  12. Ferrari SF, Pereira WLA, Santos RR, Veiga LM (2003) Fatal attack of a Boa constrictor on a bearded Saki (Chiropotes satanas utahicki). Neuropsychobiology 75:111–113. https://doi.org/10.1159/000076272

    Article  Google Scholar 

  13. Filho PRM (2015) Evolução do hábito alimentar e utilização do substrato pelo gênero Philodryas Wagler, 1830. Dissertação de mestrado. Universidade Estadual Paulista Júlio de Mesquita Filho. São Paulo: Universidade Estadual Paulista Júlio de Mesquita Filho Press. https://repositorio.unesp.br/handle/11449/127763. Accessed 11 July 2019

  14. Hasegawa T, Hiraiwa M, Nishida T, Takasaki H (1983) New evidence on scavenging behavior in wild chimpanzees. Curr Anthropol 24:231–232. https://doi.org/10.1086/202974

    Article  Google Scholar 

  15. Headland TN, Greene HW (2011) Hunter-gatherers and other primates as prey, predators, and competitors of snakes. Proc Natl Acad Sci 108:E1470–E1474. https://doi.org/10.1073/pnas.1115116108

    Article  PubMed  Google Scholar 

  16. Heymann EW (1987) A field observation of predation on a moustached tamarin (Saguinus mystax) by an anaconda. Int J 8:193–195. https://doi.org/10.1007/BF02735163

    Article  Google Scholar 

  17. Isbell L (2006) Snakes as agents of evolutionary change in primate brains. J Hum Evol 51:1–35. https://doi.org/10.1016/j.jhevol.2005.12.012

    Article  PubMed  Google Scholar 

  18. Lins P (2015) Preferência e Competição alimentar em um grupo de Sapajus flavius em fragmento de Mata Atlântica em Caaporã-Goiana–Paraiba–Brasil. Dissertação de mestrado. Universidade Federal do Rio Grande do Norte, Brasil. Universidade Federal do Rio Grande do Norte. Rio Grande do Norte: Universidade Federal do Rio Grande do Norte Press. https://repositorio.ufrn.br/jspui/bitstream/123456789/20942/1/PolianaGabrieleAlvesDeSouzaLins_DISSERT.pdf. Accessed 11 July 2019

  19. Meno W, Coss RG, Perry S (2013) Development of snake-directed antipredator behavior by wild white-faced capuchin monkeys: I. Snake-species discrimination. Am J Primatol 75:281–291. https://doi.org/10.1002/ajp.22106

    Article  PubMed  Google Scholar 

  20. Ministério do Meio Ambiente (2014) Reconhece como espécies da fauna brasileira ameaçadas de extinção aquelas constantes da “Lista Nacional Oficial de Espécies da Fauna Ameaçadas de Extinção”. Brazil. http://www.icmbio.gov.br/portal/portaldabiodiversidade/50-menu-biodiversidade/6706-portarias-fauna-ameacada. Accessed 11 July 2019

  21. Natera-Mumaw M, Diasparra JP, Novoa J, Jiménez D (2008) Defensive behavior in Philodryas viridissima (Linnaeus, 1758). Herpetotropicos 4:40. https://doi.org/10.1590/S0101-81751999000100023

    Article  Google Scholar 

  22. Neco E (2015) Interações Sociais em um grupo de macaco-prego-galego, Sapajus flavius (SCHREBER, 1774) sob competição induzida por alimento, em área de Floresta Atlântica na Paraíba. Universidade Federal da Paraíba. In: Repositório Institucional da Universidade Federal da Paraíba. Paraíba: Universidade Federal da Paraíba Press

  23. Niemitz C (1973) Tarsius bancanus (Horsfields tarsier) preying on snakes. Lab Primate Newsl 12:18–19

    Google Scholar 

  24. Perry S, Manson JH, Dower G, Wikberg E (2003) White-faced capuchins cooperate to rescue a groupmate from a Boa constrictor. Folia Primatol 74:109–111. https://doi.org/10.1159/000070008

    Article  PubMed  Google Scholar 

  25. Pessoa TSA, Neco EC, Valença-Montenegro MM (2018) A utilização do macaco-prego-galego (Sapajus flavius, Schreber, 1774) como zooterápico no Território Indígena Potiguara, na Paraíba, Brasil. In: Lucena RFP de, Lucena CM de, Carvalho TKN, Ferreira EC (eds) Plantas e Animais Medicinais da Paraíba: Visões da Etnobiologia e Etnoecologia, 1st edn. Editora IESP, Cabedelo, pp 240–251. https://www.iesp.edu.br/sistema/uploads/arquivos/publicacoes/plantas-e-animais-medicinais-da-paraiba-visoes-da-etnobiologia-e-etnoecologia.pdf. Accessed 11 July 2019

  26. Pinto LP (2008) Ecologia alimentar do cuxiú-de-nariz-vermelho Chiropotes albinasus (Primates: Pitheciidae) na Floresta Nacional do Tapajós. Universidade Estadual de Campinas. São Paulo: Universidade Estadual de Campinas Press. http://repositorio.unicamp.br/jspui/bitstream/REPOSIP/315845/1/Pinto_LiliamPatricia_D.pdf. Accessed 11 July 2019

  27. Pissinatti A, Chagas WN, da Cruz JB, et al (2017) Snake incident as a limiting factor in the process of reintroduction of lion tamarins to their habitat. Leontopithecus Lesson, 1840 (Callitrichidae-Primates). In: A Primatologia no Brasil, Vol. 14. Recife, pp 212–225

  28. Quintino EP, Bicca-Marques JC (2013) Predation of Alouatta puruensis by Boa constrictor. Primates 54:325–330. https://doi.org/10.1007/s10329-013-0377-z

    Article  PubMed  Google Scholar 

  29. Rodrigues KC (2013) Padrão de atividades, comportamento alimentar, exploração de habitat e área de vida de um grupo de Sapajus flavius (Schreber, 1774) (Primates, Cebidae) em um fragmento de floresta atlântica, Paraíba, Brasil. Universidade Federal da Paraíba. Paraíba: Universidade Federal da Paraíba Press. https://repositorio.ufpb.br/jspui/bitstream/tede/7631/2/arquivototal.pdf. Accessed 11 July 2019

  30. Rodrigues KC, Delfim FR, Castro CSS et al (2013) Strobilurus torquatus Wiegmann, 1834 (Squamata:Tropiduridae): New records from the Brazilian State of Paraíba and a geographic distribution map. Check List 9:614–617. https://doi.org/10.15560/9.3.614

    Article  Google Scholar 

  31. Santos A (2013) Padrão de forrageamento de Cebus flavius (Schreber, 1774) (Primates: Cebidae), em um fragmento de Mata Atlântica na Paraíba. Universidade Federal de Sergipe. Sergipe: Universidade Federal de Sergipe Press. https://ri.ufs.br/bitstream/riufs/4406/1/ALLINNY_COSTA_ARAUJO_SANTOS.pdf. Accessed 11 July 2019

  32. Silva GAO, Valença-Montenegro M (2017) Primatas ameaçados no Corredor Pacatuba-Gargaú, Paraíba: aspectos populacionais e uso de espaço. In: Bacellar AEF, Albuquerque EMM de, Oliveto FA, et al. (eds) Anais do IX Seminário de Pesquisa e IX Encontro de Iniciação Científica do Instituto Chico Mendes de Conservação da Biodiversidade: ICMBIO - 10 anos de aprendizado em pesquisa para a conservação. Seminário de Pesquisa e Iniciação Científica do Instituto Chico Mendes de Conservação da Biodiversidade, Brasília, p 116–117. http://icmbio.gov.br/portal/images/stories/ANAIS_DO_SEMIN%C3%81RIO_2017.pdf. Accessed 11 July 2019

  33. Takahata Y, Hiraiwa-Hasegawa M, Takasaki H, Nyundo R (1986) Newly acquired feeding habits among the chimpanzees of the Mahale Mountains National Park, Tanzania. Hum Evol 1:277–284. https://doi.org/10.1007/BF02436585

    Article  Google Scholar 

  34. Tello NS, Huck M, Heymann EW (2002) Boa constrictor attack and group defense in moustached tamarins (Saguinus mystax). Folia Primatol 73:146–148. https://doi.org/10.1159/000064795

    Article  PubMed  Google Scholar 

  35. Valença-Montenegro MM, Bezerra B, Martins A, Fialho MS (2015) Avaliação do Risco de Extinção de Sapajus flavius (Schreber, 1774) no Brasil. In: Lista de Espécies ameaçadas. http://www.icmbio.gov.br/portal/faunabrasileira/lista-de-especies/7272-mamiferos-sapajus-flavius-macaco-prego-galego. Accessed 11 July 2019

  36. Van Schaik C, Brockman D (2005) Seasonality in primate ecology, reproduction, and life history: an overview. In: Brockman D, Schaik C (eds) Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge University Press, Cambridge, pp 3–20. https://doi.org/10.1017/cbo9780511542343.002

    Chapter  Google Scholar 

  37. Vitale AF, Visalberghi E, De Lillo C (1990)Responses to a model snake in captive crab-eating macaques (Macaca fascicularis) and tufted capuchins (Cebus apella): a comparison. Ethol Ecol Evol 2(3):333–334. https://doi.org/10.1080/08927014.1990.9525479

    Article  Google Scholar 

  38. Vitt LJ, Vangilder LD (1983) Ecology of a snake community in northeastern Brazil. Amphibia-Reptilia 4:273–296. https://doi.org/10.1163/156853883X00148

    Article  Google Scholar 

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Acknowledgements

We are grateful to the Centro Nacional de Pesquisa e Conservação de Primatas Brasileiros and Instituto Chico Mendes de Conservação da Biodiversidade (CPB/ICMBio) and all their members, to the Laboratory of Mastozoology (MAME) particularly to Mr. Pedro Cordeiro Estrela, and to Laboratory of Applied Ecology and Conservation (LEAC) both from Department of Systematics and Ecology−University Federal of Paraíba. Thanks to Mr. Lucas Cavalcanti, Mr. Fagner Delfim, and the Herpetology Laboratory of University Federal of Paraíba for the snake identification and references, and to Monte Alegre, the owner of Sucupira torta, for all of the support given during the data collection. We are grateful to Mr. William McGrew and other reviewers from Primates, and to Ms. Illiana E. Anise for their very helpful suggestions for the improvement of this paper. Special thanks to the Brazilian Society of Primatology, to Mr. Tarcísio Alves Cordeiro, Mr. Ronilson José da Paz, and Mr. Adelson, a great field partner, without whose help this work would not have been possible.

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Da Silva, G.A.O., Falótico, T., Nash, S.D. et al. A green racer snake (Philodryas nattereri, Colubridae) killed but not eaten by a blonde capuchin monkey (Sapajus flavius, Cebidae). Primates 60, 459–465 (2019). https://doi.org/10.1007/s10329-019-00738-9

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Keywords

  • Interspecific interaction
  • Competition
  • Prey
  • Predation
  • Snake detection
  • Sapajus flavius