Abstract
Although primate predation is rarely observed, a series of primate anti-predation strategies have been described. Energetic costs of such strategies can vary from high-cost mobbing, via less costly alarm calling, to low-cost furtive concealment. Here we report the anti-predation strategies of red-nosed cuxiú, Chiropotes albinasus, based on direct observations from four study sites in southeastern Brazilian Amazonia. Over a collective period of 1255 fieldwork hours, we observed nine direct interactions between raptors (all potential predators) and red-nosed cuxiús. Of these, one (11%) resulted in predation. Raptors involved were: Harpia harpyja (four events), Leucopternis sp. (two events), Spizaëtus tyrannus (one event), and unidentified large raptors (two events). Predation attempts occurred in flooded-forest and terra firme rainforest, were directed at both adult and non-adult cuxiús, and involved both adult and juvenile raptors. Anti-predation strategies adopted by the cuxiús included: (1) group defence and mobbing behaviour (two occasions), (2) dropping into dense sub-canopy (seven occasions), (3) alarm calling (eight occasions), and (4) fleeing to, and hiding in, dense vegetation (eight occasions). During each encounter at least two of these behaviours were recorded. These are the first published records of predation, predation attempts, and anti-predator behaviour involving red-nosed cuxiú.
Similar content being viewed by others
References
Aguiar-Silva FH, Sanaiotti TM, Luz BB (2014) Food habits of the harpy eagle, a top predator from the Amazonian rainforest canopy. J Raptor Res 48:24–35
Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49:227–267
Arlet ME, Isbell LA (2009) Variation in behavioral and hormonal responses of adult male gray-cheeked mangabey (Lophocebus albigena) to crowned eagles (Stephanoaetus coronatus) in Kibale National Park, Uganda. Behav Ecol Sociobiol 63:491–499
Ayres JM (1981) Observacoes sobre a ecologia e o comportamento dos cuxius (Chiropotes albinasus e Chiropotes satanas, Cebidae: Primates). Masterʼs Thesis, Universidade do Amazonas: Manaus. pp 142
Ayres JM, Milton K (1981) Levantamento de primatas e habitat no Rio Tapajós. Bol Mus Paraense Emilio Goeldi N. S Zool. 111:1–11
Barlow J, Haugaasen T, Peres C (2002) Sympatry of the black-faced Hawk Leucopternis melanops and the white-browed Hawk Leucopternis kuhli in the lower Rio Tapajós, Pará, Brazil. Cotinga 18:77–79
Barnett AA, Schiel V, Deveny A, Valsko J, Spironello WR, Ross C (2011) Predation on Cacajao ouakary and Cebus albifrons (Primates: Platyrrhini) by harpy eagles. Mammalia 75:169–172
Barnett AA, Almeida T, Spironello WR, Sousa Silva W, MacLarnon A, Ross C (2012a) Terrestrial foraging by Cacajao melanocephalus ouakary (Primates) in Amazonian Brazil: is choice of seed patch size and position related to predation-risk? Folia Primatol 83:126–139
Barnett AA, Shaw P, Spironello WR, MacLarnon A, Ross C (2012b) Sleeping site selection by golden-backed uacaris, Cacajao melanocephalus ouakary (Pitheciidae), in Amazonian flooded forests. Primates 53:273–285
Barnett AA, Andrade E, Ferreira MC, da Silva VF, Oliveira T (2015) Primate predation by black hawk-eagle (Spizaetus tyrannus) in Brazilian Amazonia. J Raptor Res 49:105–107
Bezerra BM, Barnett AA, Souto A, Jones G (2009) Predation by the tayra on the common marmoset and the pale-throated three-toed sloth. J Ethol 27:91–96
Bezerra BM, Souto AS, Jones G (2010) Vocal repertoire of golden-backed uakaris (Cacajao melanocephalus): call structure and context. Int J Primatol 31:759–778
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
Boinski S, Treves A, Chapman C (2000) A critical evaluation of the influence of predators on primates: effects on group travel. In: Boinski S, Garber PA (eds) On the Move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 43–72
Boinski S, Kauffman L, Westoll A, Stickler CM, Cropp S, Ehmke E (2003) Are vigilance, risk from avian predators and group size consequences of habitat structure? A comparison of three species of squirrel monkey (Saimiri oerstedii, S. boliviensis, and S. sciureus). Behaviour 140:1421–1467
Branch LC (1983) Seasonal and habitat differences in the abundance of primates in the Amazon (Tapajós) National Park, Brazil. Primates 24:424–431
Calquhoun IC (2007) Anti-predator strategies of cathemeral primates: dealing with predators of the day and the night. In: Gursky-Doyen S, Nekaris KAI (eds) Primate anti-predator strategies. Springer, New York, pp 146–172
Caro T (2005) Mobbing and group defense. In: Caro T (ed) Anti-predator defenses in birds and mammals Chicago. University of Chicago Press, Chicago, pp 381–411
Cäsar C, Bryne RW, Hoppitt W, Zuberbühler K Young RJ (2012) Evidence for semantic communication in titi monkey alarm calls. Anim Behav 84:405–411
Chapman CA (1986) Boa constrictor predation and group response in white-faced Cebus monkeys. Biotropica 18:171–172
Cheney DL, Wrangham RW (1987) Predation. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate Societies. University of Chicago Press, Chicago, pp 227–239
Cowlishaw G (1994) Vulnerability to predation in baboon populations. Behaviour 131:293–304
de Luna AG, SanMiguel R, Di Fiore A, Fernandez-Duque E (2010) Predation and predation attempts on red titi monkeys (Callicebus discolor) and Equatorial sakis (Pithecia aequatorialis) in Amazonian Ecuador. Folia Primatol 81:86–95
de Oliveira TG, Mazim FD, Vieira OQ, Barnett APA, Silva GN, Soares JBG, Santos JP, da Silva VF, Araújo PF, Tchaika L, Miranda CL (2016) Nonvolant mammal megadiversity and conservation issues in a threatened central Amazonian hotspot in Brazil. Trop Cons Biol 2016:1–16. doi:10.1177/1940082916672340
de Souza Martins S, de Lima EM, de Sousa e Silva J (2005) Predation of a bearded saki (Chiropotes utahicki) by a harpy eagle (Harpia harpyja). Neotrop Primates 13:7–10
Ferrari SF (1995) Observations on Chiropotes albinasus from the Rio dos Marmelos, Amazonas, Brazil. Primates 36:289–293
Ferrari SF (2009) Predation risk and antipredator strategies. In: Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB (eds) South American Primates. Springer, New York, pp 251–277
Ferrari SF, Port-Carvalho M (2003) Predation of an infant collared peccary by a Harpy Eagle in eastern Amazonia. Wilson Bull 115:103–104
Ferrari SF, Iwanga S, Coutinho PEG, Messias MR, Cruz Neto EH, Ramos EM, Ramos CS (1999) Zoogeography of Chiropotes albinasus (Platyrrhini, Atelidae) in southwestern Amazonia. Int J Primatol 20:995–1004
Ferrari SF, Iwanaga S, Ravetta AL, Freitas FC, Souza BAR, Souza LL, Costa CC, Coutinho PEG (2003) Dynamics of primate communities along the Santarém-Cuiabá highway in south-central Brazilian Amazonia. In: Marsh L (ed) Primates in fragments: ecology and conservation. Kluwer Academic/Plenum Publishers, New York, pp 123–144
Ferrari SF, Pereira WLA, Santos RS, Veiga LM (2004) Fatal attack of a Boa constrictor on a bearded saki (Chiropotes satanas utahicki). Folia Primatol 75:111–113
Ferreira LV, Prance GT (1998) Structure and species richness of low-diversity floodplain forest on the Rio Tapajós, Eastern Amazonia, Brazil. Biodiv Cons 7:585–596
Fichtel C (2007) Avoiding predators at night: antipredator strategies in red-tailed sportive lemurs (Lepilemur ruficaudatus). Am J Primatol 69:611–624
Frechette JL, Sieving KE, Boinski S (2014) Social and personal information use by squirrel monkeys in assessing predation risk. Am J Primatol 76:956–966
Galetti M (1996) Comportamentos anti-predatórios em quatro espécies de Primatas no sudeste do Brasil. Rev Bras Biol 56:203–206
George TK, Marques SA, de Vivo M, Branch LC (1988) Valentões dos mamíferos do Parna-Tapajós. Brasil Florestal 63:33–41
Gilbert KA (2000) Attempted predation on a white-faced saki in the Central Amazon. Neotrop Primates 8:103–104
Gursky-Doyen S, Nekaris KAI (eds) (2007) Primate anti-predator strategies. Springer, New York
Hershkovitz P (1985) A preliminary taxonomic review of the South American bearded saki monkeys genus Chiropotes (Cebidae, Platyrrhini), with the description of a new subspecies. Fieldiana Zool N. S. 27:1–46
Heymann EW (1990) Reactions of wild tamarins, Saguinus mystax and Saguinus fuscicollis to avian predators. Int J Primatol 11:327–337
Howell SNG, Webb S (1995) A guide to the birds of Mexico and Northern Central America. Oxford University Press, Oxford
Isbell L (1994) Predation on primates: ecological patterns and evolutionary consequences. Evol Anthropol 3:61–71
IUCN (2015) The IUCN red list of threatened species. Version 2015.3. http://www.iucnredlist.org
Lehner B, Verdin K, Jarvis A (2006) HydroSHEDS technical documentation. World Wildlife Fund US, Washington, DC. Available at http://hydrosheds.cr.usgs.gov
Lenz BB, dos Reis AM (2011) Harpy Eagle–primate interactions in the central Amazon. Wilson J Ornithol 123:404–408
Lledo-Ferrer Y, Hidalgo A, Heymann EW, Peláez F (2009) Field observation of predation of a Slate-colored Hawk, Leucopternis schistacea, on a juvenile saddle-back tamarin, Saguinus fuscicollis. Neotrop Primates 16:82–84
Matsuda I, Izawa K (2008) Predation of wild spider monkeys at La Macarena, Colombia. Primates 49:65–68
Matsumoto-Oda A (2015) How surviving baboons behaved after leopard predation: a case report. Anthropol Sci 123:13–17
McKinney T (2009) Anthropogenic change and primate predation risk: crested Caracaras (Caracara plancus) attempt predation on mantled howler monkeys (Alouatta palliata). Neotrop Primates 16:24–27
Miranda JDM, Bernardi IP, Moro-Rios RF, Passos FP (2006) Antipredator behaviour of brown howlers attacked by black hawk-eagle in southern Brazil. Int J Primatol 27:1097–1101
Mourthé I (2011) Reactions of white-bellied spider monkeys to a predation attempt by a cougar. Neotrop Primates 18:28–29
Mourthé I, Barnett AA (2014) Crying Tapir: the functionality of errors and accuracy in predator recognition in two Neotropical high-canopy primates. Folia Primatol 85:379–398
Oren DC, Parker TA III (1997) Avifauna of the Tapajós National Park and vicinity, Amazonian Brazil. Ornithol Monogr 48:493–525
Passamani M (1995) Field observation of a group of Geoffroys marmosets mobbing a Margay cat. Folia Primatol 64:163–166
Peetz A (2001) Ecology and social organization of the bearded saki Chiropotes satanas chiropotes (Primates: Pitheciinae) in Venezuela. Ecotrop Monogr 1:1–170
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
Pinto IP (2008) Ecologia alimentar do cuxiú-de-nariz-vermelho Chiropotes albinasus (Primates: Pitheciidae) na Floresta Nacional do Tapajós, Doctoral thesis, Universidade Estadual de Campinas, Campinas (Brazil)
Prance GT (1979) Notes on the vegetation of Amazonia III. The terminology of Amazonian forest types subject to inundation. Brittonia 31:26–38
Quinn JL, Cresswell W (2004) Predator hunting behaviour and prey vulnerability. J Animal Ecol 73:143–154
Ribeiro-Júnior MA, Ferrari SF, Lima JRF, da Silva CR, Lima JD (2016) Predation of a squirrel monkey (Saimiri sciureus) by an Amazon tree boa (Corallus hortulanus): even small boids may be a potential threat to small-bodied platyrrhines. Primates. doi:10.1007/s10329-016-0545-z:1-6
Riley CM, Koenig BL, Gumart MD (2015) Observation of a fatal attack on a juvenile long-tailed macaque in a human-modified environment in Singapore. Nat Singapore 8:57–63
Rocha EC, Silva E (2013) Tamanho de grupos e densidade populacional de primatas na região do Cristalino, Amazônia Meridional brasileira. Rev Bras Biociências 11:301–306
Rose LM, Perry S, Panger MA, Jack K, Manson JH, Gros-Louis J, MacKinnon KC, Vogel E (2003) Interspecific interactions between Cebus capucinus and other species: data from three Costa Rican sites. Int J Primatol 24:759–796
Scheumann M, Rabesandratana A, Zimmerman E (2007) Predation, communication and cognition in lemurs. In: Gursky-Doyen S, Nekaris KAI (eds) Primate anti-predator strategies springer. US, NewYork, pp 100–126
Shahuano-Tello N, Huck M, Heymann EW (2002) Boa constrictor attack and successful group defence in moustached tamarins, Saguinus mystax. Folia Primatol 73:146–148
Silva FHA (2007) Dieta do gavião-real Harpia harpyja (Aves: Accipitridae) em florestas de terra firme de Parintins, Amazonas, Brasil. Masters dissertation, Instituto Nacional de Pesquisas da Amazonas (Brazil)
Soares da Silva RF (2013) Comportamento e dieta de Chiropotes albinasus (I. Geoffroy & Deville, 1848), cuxiú-de-nariz-vermelho. Masters dissertation, Museu Paraense Emílio Goeldi and Universidade Federal do Pará (Brazil)
Stanford CB (2002) Avoiding predators: expectations and evidence in primate antipredator behavior. Int J Primatol 23:741–757
Stone AI (2007) Age and seasonal effects on predator-sensitive foraging in squirrel monkeys (Saimiri sciureus): a field experiment. Am J Primatol 69:127–141
Suscke P, Verderane M, de Oliveira RS, Delval I, Fernández-Bolaños M, Izar P (2016) Predatory threat of harpy eagles on yellow-breasted capuchin monkeys in the Atlantic Forest. Primates. doi:10.1007/s10329-016-0557-8
Teixeira DS, dos Santos E, Leal SG, de Jesus AK, Vargas WP, Dutra I, Barros M (2016) Fatal attack on black-tufted-ear marmosets (Callithrix penicillata) by a Boa constrictor: a simultaneous assault on two juvenile monkeys. Primates 57:123–127
Tórrez L, Robles N, González A, Crofoot MC (2012) Risky business? Lethal attack by a jaguar sheds light on the costs of predator mobbing for capuchins (Cebus capucinus). Int J Primatol 33:440–446
Urbani B, Kvarnbäck J, González-Alentorn GA (2012) Harpy eagle Harpia harpyja preying on an ursine howler monkey Alouatta arctoidea in northeastern Venezuela. Rev Catalana Ornitol 28:40–44
Vasquez MRO, Heymann EW (2001) Crested eagle (Morphnus guianensis) predation on infant tamarins (Saguinus mystax and Saguinus fuscicollis, Callitrichinae). Folia Primatol 72:301–303
Vaz SM (2001) Primatas da região do Rio Tapajós, Pará, Brasil. Neotrop Primates 9:54–57
Veiga LM, Ferrari SF (2013) Ecology and behavior of bearded sakis (genus Chiropotes). In: Veiga LM, Barnett AA, Ferrari SF, Norconk MA (eds) Evolutionary biology and conservation of titis, sakis and uacaris. Cambridge University Press, Cambridge, pp 240–249
Wallace RB, Painter RLE, Taber AB, Ayres JM (1996) Notes on a distributional river boundary and southern range extension for two species of Amazonian primates. Neotrop Primates 4:149–151
Acknowledgements
AAB, JMS thank Maracajá Ecological Consulting (MEC) for the invitation to conduct the survey work. TdeO wishes to thank CNEC/WorleyParsons and ELETROBRÁS for financial support of the mammal survey in the Tapajós river basin. We also thank MEC’s Gitana Cavalcanti for retrieving essential data. LPP and EZS thank Ibama and TNF coordinators, field guides Herrison and Adailson, Fundação de Amparo à Pesquisa do Estado de São Paulo (03/06256-5), Fundação O Boticário de Proteção à Natureza, and the Primate Action Fund of Conservation International. RFSS thanks Ana C Mendes and Liza Maria Veiga (in memoriam), Cristalino Jungle Lodge, Museu Paraense Emílio Goeldi/Universidade Federal do Pará, fieldguide Leandro Pereira, and CNPQ for financial support. Collectively, we thank Stuart Semple (Roehampton U.) for comments on call type phylogeny. Adrian Barnett dedicates this paper to the memory of Donald Petrie (1958–2014), a fine and dedicated birder. This paper is contribution 12 from the Amazon Mammal Research Group, and contribution number 23 from the Igapó Study Project.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Barnett, A.A., Silla, J.M., de Oliveira, T. et al. Run, hide, or fight: anti-predation strategies in endangered red-nosed cuxiú (Chiropotes albinasus, Pitheciidae) in southeastern Amazonia. Primates 58, 353–360 (2017). https://doi.org/10.1007/s10329-017-0596-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-017-0596-9