Open Access
How to translate text using browser tools
1 December 2014 Bird Predation by an Endangered Primate Species, Callicebus Coimbrai, in the Brazilian Atlantic Forest
Luana Vinhas, João Pedro Souza-Alves
Author Affiliations +

The world faces a significant environmental crisis, in which continuous natural environments are being reduced to disturbed fragments (Ladle and Whittaker, 2011). Some species can take advantage of this process, but the majority of biodiversity is threatened by human activities (IUCN, 2012). Ecological plasticity is regarded as a characteristic that favors species' survival when habitat becomes degraded (McKinney, 1997). Most primates have generalist diets and show some behavioral plasticity (Garber, 1987); however, current knowledge is concentrated on some well studied species, while there is a lack of information for other primates.

Titi monkeys (Callicebus spp.) are regarded as primarily frugivorous primates that complement their diets with invertebrate prey and other plant parts, such as leaves, seeds and flowers (Bicca-Marques and Heymann, 2013; DeLuycker, 2012; Heymann and Nadjafzadeh, 2013). These primates tolerate disturbed habitat (Heiduck, 2002; Jerusalinsky et al., 2006; Souza-Alves et al. 2011a) and it has been suggested already that titi monkeys might show some dietary plasticity. For example, Santos et al. (2012) report that C. nigrifrons can take advantage of temporarily available items, such as synchronous production of seed bamboo (=masting bamboos). Neri (1997) describes a male C. personatus driving a dove away from its nest and allowing the female to eat its egg. Souza-Alves et al. (2011b) verified a high consumption of insects (i. e., caterpillars) during the dry season by C. coimbrai. However, up to now, there are no reports of titis preying on vertebrates.

Here, we report bird predation by one sub adult C. coimbrai in a large fragment of Atlantic forest in the northeastern Brazil. The observation appears to be the first record of predation of birds by C. coimbrai and by titis in general. The events occurred in the largest fragment of the Mata do Junco Wildlife Refuge - MJWR (10°32′S, 37°03′W), which encompasses 522 ha of Atlantic Forest in the municipality of Capela, state of Sergipe, in northeastern Brazil. Systematic monitoring of the C. coimbrai study group has occurred since 2011 until the present time (Chagas et al., 2013). Between January and March 2014 — when the event was recorded — quantitative behavioral data were collected in scan samples at 5-min intervals. In March 2014, when the events were observed, the study group was composed of a breeding pair, one subadult/adult, two juveniles and one infant.


On March 5th 2014, at approximately 14:50 h, one subadult Callicebus coimbrai was observed preying on a nestling Pale-breasted Thrush (Turdus leucomelas, Turdidae). The nest was among the branches and foliage at 3 m of height and fixed on a branch of a Guapira opposita tree. The titi monkey grabbed its prey with the right hand and started eating it 1 m away from the nest. Two other individuals of T. leucomelas - probably the nestling parents - were observed vocalizing intensely nearby. Afterwards, one of the birds tried unsuccessfully to drive the titi away from its nest by attacking the titi's head. The birds continued vocalizing near the nest for approximately four minutes. The titi monkey seemed distressed with the approach of one MJWR employee and moved away from the area after dropping the rest of the nestling body to the ground (Fig- 1).

One day later, at approximately 10:30 h, the same individual was observed preying on another T. leucomelas nestling in the same nest. Once again, the titi held its prey with the right hand and ate it at the exact same place. The consumption of the prey lasted for approximately six minutes; meanwhile two T. leucomelas individuals flew around and vocalized some 8 m away, without approaching the titi. After eating the nestling, the titi moved away from the area together with other group members. Curiously, one adult male of the same C. coimbrai group was observed destroying abandoned nests on two occasions at Mata do Junco and during the monitoring in March 2014, the same individual of the records above was observed preying on eggs in the nest of an unidentified bird species.

Figure 1.

Photograph of the remains of two individuals of Turdus leucomelas preyed by Callicebus coimbrai at the Mata do Junco Wildlife Refuge.



The predation of birds by primate species has been recorded widely in the literature. Marmosets (Callithrix spp.) were observed preying on bird eggs and nestlings of at least 15 species, including T. leucomelas (Mendes Pontes and Soares, 2005; Lyra-Neves et al., 2007; Begoti and Landsemann, 2008; Gomes and Lima-Gomes, 2011; Alexandrino et al., 2012). In addition, capuchins (Sapajus spp.) were also observed preying on Harpiprion caerulescens and Ictinia plumbea (Olmos, 1990) and specifically S. apella was observed in 24 predation events (Ferreira et al., 2002). Woolly monkeys captive (Lagothrix lagotricha) has been recorded preying birds in 15 events (Stearns et al., 1988). Estrada and Estrada (1977) have recorded bird predation by stump tail macaques (Macaca arctoides) and, also chimpanzees (Pan troglodytes schweinfurthii) preyed 15 birds species or their eggs at Mahale Mountains, Tanzania (Nishida and Uehara 1983). Other birds, such as hawks, kites, toucans, and jays; arboreal snakes; and mammals, such as coatis, opossums, and primates are among the potential predators of bird eggs and nestlings in forest fragments (Morre and Robinson, 2004).

In the literature, titi monkeys have been commonly regarded as prey of other vertebrates. For example, there are records of predation of Callicebus spp. by crested eagles (Morphnus guianensis, Terborgh, 1983), capuchin monkeys (Sapajus apella, Sampaio and Ferrari, 2005; Cebus spp., Lawrence, 2003), ocelot (Leopardus pardalis, Bianchi, 2001; Bianchi and Mendes, 2007), Boa constrictor (Cisneros-Heredia et al., 2005), margay (Leopardus wiedii, Defler, 2004) and harpy eagles (Harpy harpyja, de Luna et al., 2010). Nest predation can negatively impact bird richness and diversity (Argel de Oliveira, 1995); however, given its rarity, predation of birds by titis seems likely to have little effect on bird populations.

The study group have a diet based mainly on fruits and vegetative plant parts (Chagas et al., 2013), which is typical for the genus (Bicca-Marques and Heymann, 2013). However, there are two possible explanations for the absence of other reports of bird predation by titis. First, other titi groups may also prey opportunistically on birds, but this may not have been observed by other researchers given the rarity of these events. Secondly, bird predation may be a response of the study group to habitat degradation. Both potential explanations highlight the possible plasticity and opportunism of titi monkeys, and help our understanding of the persistence of these monkeys in highly degraded landscapes, such as the Atlantic Forest of Northeastern Brazil.


JPS-A is grateful to CNPq for a Postdoctoral Fellowship (Process no. 163414/2013-0). The Sergipe State Environment Secretariat (SEMARH) provided additional logistic support. We also thank Marcelo José and Marcelo Silva, for their assistance during fieldwork. We are also grateful to Renato Hilário, Stuart Semple and Jessica Lynch Alfaro for valuable suggestions on early drafts of the manuscript.



E. R. Alexandrino , D. T. A. Luz , E. V. Maggiorini & K. M. P. M. B. Ferraz 2012. Nest stolen: the first observation of nest predation by an invasive exotic marmoset (Callithrix penicillata) in an agricultural mosaic. Biota Neotrop. 12: 211–215 Google Scholar


M. M. Argel-de-Oliveira 1995. Aves e vegetação em um bairro residencial da cidade de São Paulo (São Paulo, Brasil). Rev. Brasil. Zool. 12(1): 81– 92. Google Scholar


R. A. Begotti and L. F. Landesmann 2008. Predação de ninhos por um grupo híbrido de Saguis (Callithrix jacchus/penicillata) introduzidos em área urbana: implicações para a estrutura da comunidade. Neotrop. Primates. 15: 28–29 Google Scholar


R. C. Bianchi 2001. Estudo comparativo da dieta da jaguatirica, Leopardus pardalis (Linnaeus, 1758), em Mata Atlântica Dissertação de Mestrado, Universidade Federal do Espírito Santo, Vitória. Google Scholar


R. D. C. Bianchi and S. L. Mendes 2007. Ocelot (Leopardus pardalis) predation on primates in Caratinga Biological Station, Southeast Brazil. Am. J. Primatol. 69: 1173–1178. Google Scholar


J. C. Bicca-Marques and E.W. Heymann 2013. Ecology and Behaviour of titi monkey (genus Callicebus). In: Evolutionary Biology and Conservation of Titis, Sakis, and Uacaris, A. A. Barnett , L. M. Veiga , S. F. Ferrari , and M. A. Norconk (eds.), pp. 196–207. Cambridge University Press. Google Scholar


R. R. D. Chagas , M. M. Santana , J. P. Souza-Alves and S. F. Ferrari 2013. Seasonal variation in the diet of Callicebus coimbrai (Platyrrhini: Pitheciidae) in the Mata do Junco Wildlife Refuge, northeastern Brazil. In: Anais do II Congresso Latino Americano e XV Congresso Brasileiro de Primatologia, Recife, Pernambuco, Brasil. Google Scholar


D. Cisneros-Heredia , A. Leon-Reyes and S. Seger 2005. Boa constrictor predation on a titi monkey, Callicebus discolor. Neotrop. Primates. 13:11–12. Google Scholar


T. Defler 2004. Primates de Colombia. Bogotá, Conservación International. Google Scholar


A. G. De Luna , R. Sanmiguel , A. Di Fiori and E. F. Duque 2010. Predation and predation attempts on red titi monkeys (Callicebus discolor) and equatorial sakis (Pithecia aequatorialis) in Amazonian Ecuador. Folia Primatol. 81: 86–95. Google Scholar


A. M. DeLuycker 2012. Insect prey foraging strategies in Callicebus oenanthe in Northern Peru. Am. J. Primatol. 74: 450–461. Google Scholar


A. Estrada and R. Estrada 1977. Pattern of predation in a free-ranging troop of stumptail macaques (Macaca arctoides): Relations to the Ecology II. Primates , 18:633–646. Google Scholar


R. Ferreira , B. D. Resende , M. Mannu , E. B. Ottoni and P. Izar 2002. Bird predation and prey-transfer in brown capuchin monkeys (Cebus apella). Neotrop. Primates. 10:84–89. Google Scholar


P. A. Garber 1987. Foraging strategies among living primates. Ann. Rev. Anthropol. 16: 339–364. Google Scholar


F. B. R. Gomes and R. C. Lima-Gomes 2011. Registro ocasional da predação da pomba-de-bando (Zenaida auriculata des Murs, 1847) pelo sagüi-do-cerrado (Callithrix penicillata é. Geoffroy, 1812) no interior de São Paulo,SP. Neotrop. Primates. 18: 68–70. Google Scholar


S. Heiduck 2002. The use of disturbed and undisturbed forest by marked titi monkey Callicebus personatus melanochir is proportional to food availability. Oryx , 36:133–139. Google Scholar


E. W. Heymann and M. Nadjafzadeh 2013. Insectivory and prey foraging in titi monkeys - a case study of Callicebus cupreus and a comparison to other pitheciids. In: Evolutionary Biology and Conservation of Titis, Sakis and Uacaris. A. A. Barnett , L. M. Veiga , S. F. Ferrari , and M. A. Norconk (eds.), pp.215–224. Cambridge University Press. Google Scholar


IUCN. 2012. Highlights of the 2012 IUCN World Conservation Congress. Google Scholar


L. Jerusalinsky , M. M. Oliveira , R. F. Pereira , V. Santana , P. C. R. Bastos and S. F. Ferrari 2006. Preliminary evaluation of the conservation status of Callicebus coimbrai (Kobayashi &Langguth, 1999) in the Brazilian state of Sergipe. Primate Conservation. 21: 25–32. Google Scholar


R. J. Ladle and R. J. Whittaker 2011. Conservation biogeography. Wiley-Blackwell, Oxford. Google Scholar


J. Lawrence 2003. Preliminary report on the natural history of brown titi monkeys (Callicebus brunneus) at Los Amigos Research Station, Madre de Dios, Peru. Am. J. Phys. Anthropol. Supplement 36: 136. Google Scholar


R. M. Lyra-Neves , M. A. Oliveira , W. R. Telino-Júnior , and E. M. Santos 2007. Comportamentos interespecíficos entre Callithrix jacchus (Linnaeus) (Primates, Callitrichidae) e algumas aves de Mata Atlântica, Pernambuco, Brasil. Rev. Brasil. Zool. 24 (3): 709–716. Google Scholar


M. L. McKinney 1997. Extinction vulnerability and selectivity: combining ecological and paleontological views. An. Rev. Ecol. Syst. 28.1: 495–516. Google Scholar


A. R. Mendes Pontes and M. L. Soares 2005. Sleeping sites of common marmosets (Callithrix jacchus) in defaunated urban forest fragments: a strategy to maximize food intake. J. Zool. 266: 55–63. Google Scholar


R. P. Morre and D. Robinson 2004. Artificial bird nests, external validity, and bias in ecological field studies. Ecology , 85: 1562–1567. Google Scholar


F. M. Neri 1997. Manejo de Callicebus personatus, Geoffroy 1812, resgatados: Uma tentativa de reintrodução e estudos ecológicos de um grupo silvestre na Reserva do Patrimônio Natural Galheiro - Minas Gerais. Dissertação de Mestrado, Universidade Federal de Minas Gerais. Google Scholar


T. Nishida and S. Uehara Natural diet of chimpanzés (Pan trogloditys schweinfurthii): Long-term record from the Mahale Mountains, Tanzania. Afr. Studies 3:109–130. Google Scholar


D. T. Sampaio and S. F. Ferrari 2005. Predation of an infant titi monkey (Callicebus moloch) by a tufted capuchin (Cebus apella). Folia Primatol. 76(2): 113–155. Google Scholar


G. P. Santos , C. Galvão and R. J. Young 2012. The diet of wild black-fronted titi monkeys Callicebus nigrifrons during a bamboo masting year. Primates. 53: 265–272. Google Scholar


J. P. Souza-Alves , I. P. Fontes and S. F. Ferrari 2011a. Use of sleeping sites by a titi monkey group (Callicebus coimbrai) in the Brazilian Atlantic Forest. Primates 52: 155–161. Google Scholar


J. P. Souza-Alves , I. P. Fontes , R. R. Chagas and S. F. Ferrari 2011b. Seasonal versatility in the feeding ecology of a group of titis (Callicebus coimbrai) in the northern Brazilian Atlantic Forest. Am. J. Primatol. 73: 1199–1209. Google Scholar


M. J. Stearns , B. C. White , E. Schneider and E. Bean 1998. Bird predation by captive woolly monkeys (Lagothrix lagotricha). Primates 29:361–367. Google Scholar


J. Terborgh 1983. Five New World Primates. Princeton, NJ, Princeton University Press. Google Scholar


F. Olmos 1990. Nest predation of plumbeous ibis by capuchin monkeys and greater black hawk. Wilson Bulletin 102(1): 169–170. Google Scholar
Luana Vinhas and João Pedro Souza-Alves "Bird Predation by an Endangered Primate Species, Callicebus Coimbrai, in the Brazilian Atlantic Forest," Neotropical Primates 21(2), 195-198, (1 December 2014).
Published: 1 December 2014
Back to Top