Introduction
Capuchin monkeys forage opportunistically and exploit highly diverse feeding resources that encompass a wide variety of vegetables and animal prey, including reproductive and non-reproductive plant parts, invertebrates and small vertebrates (Terborgh, 1983; Fedigan, 1990). Vertebrate prey includes birds, eggs, lizards, frogs, young coatis, bats, rodents and even other monkeys (Izawa, 1978; Newcomer and De Farcy, 1985; Fedigan, 1990; Galetti, 1990; Rose, 1997; Ferreira et al., 2002; Resende et al., 2003; Fragaszy et al., 2004; Sampaio and Ferrari, 2005). The foraging patterns of capuchin monkeys involve strenuous and persistent activity, search for hidden prey, manual dexterity and an explorative approach (Fedigan, 1990; Janson and Boinski, 1992; Fragaszy et al., 2004), but little is known regarding how they find and kill their prey. Here we report the behavior of Cebus cay (Illiger, 1815) (Cebus libidinosus sensu Groves, 2001; Rylands et al., 2005) preying upon arboreal rodents (Rhipidomys sp.2 sensu Tribe, 1996) trapped during a study on small mammal population ecology.
Methods and Study Site
During a capture-mark-recapture study of small rodents and marsupials, the researchers were frequently followed by a group of capuchin monkeys. On these occasions, the monkeys' behaviors were recorded ad libitum (Altmann, 1974). Trapping sessions, lasting from six to ten days, were conducted every month from March to August 2006 using live-traps. The study was conducted in Cabeceira do Prata Private Reserve, state of Mato Grosso do Sul, central Brazil (21° 27′ S; 56° 26′ W), an area of 307.5 ha covered with seasonal forest and cerrado (Brazilian Savanna). The region has a dry season from May to September and a wet season from October to April. The Reserve is intensely visited throughout the year by tourists, who walk in small, guided groups through the forest. There is no direct interaction between the animals and the tourists. However, reserve officers keep artificial feeding sites along the trails, baited daily with corn to attract animals to facilitate wildlife watching. All observations reported here were conducted in an area of seasonal alluvial forest that is cut by a tourist trail.
Results and Discussion
From the first fieldwork session in March 2006, the traps attracted the attention of capuchin monkeys, who began to follow the trapping activities almost every day. The first observation involved a capuchin running after another animal in the forest canopy on the morning of March 3rd. It was not possible to identify the chased animal, which was the size of an opossum (Didelphis albiventris Lund, 1840) and had a long and naked tail. The outcome of this interaction was not observed. On March 21st at around 7:00 a.m., a juvenile capuchin was found vocalizing loudly, trapped inside a trap set on the ground. Other capuchins were watching nearby when it was released. On April 19th a male climbing mouse, Rhipidomys sp. (weight = 65 g), was captured by a capuchin just after it was released from the trap. On this occasion the group of capuchins observed the activities of the researchers from canopy branches at a distance of about 10 m. When the rodent was released a subadult capuchin quickly approached, grabbed it as it climbed a tree in the understory, and killed it using the craniocervical bite, a widespread killing strategy adopted by other primate genera (Steklis and King, 1978). The monkey remained in the understory for about 2 minutes, licking the blood from the neck of the prey and looking at the researchers, before moving to the canopy. It was not possible to observe whether it ate the prey or not. This incident took place after a 28-day interval between trapping activities, a time when the traps had remained closed.
On August 25th another male Rhipidomys sp. (weight = 105 g) was captured by an adult male capuchin after the rodent was released from a trap. As in the previous case, capuchins observed the researchers from a distance, and when the rodent was released, one individual quickly approached. At this time, the capuchin chased the rodent on understory branches, but the Rhipidomys fell to the ground and hid inside a hole in a fallen log. The capuchin descended to the forest floor, extracted the rodent from the log and took it to a branch about 3 m above the ground (Figure 1a). The rodent didn't attempt to escape. The monkey killed the prey with a cranio cervical bite, licked its neck and face, ripped out a piece of flesh and ate it (Figure 1b). Then, the capuchin took it to the canopy where no further observation was possible. In both of these predation events the hunter was at a distance of at least 5 m from its group members and no interaction with the other capuchins was recorded. In addition to these events, we recorded 12 cases of attacks on the trapped rodents, with traps either on the forest floor or on branches in the understory. Seven attacks resulted in tail and ear mutilation, but these rodents survived. In the remaining five attacks the rodents were killed. Although it was not possible to identify the actors of these attacks, capuchin monkeys are the major suspects. It is intriguing that only rodents (total number of captures = 496) were attacked, although 166 captures of the small marsupial Gracilinanus agilis (Burmeister, 1854) were also made.
The differences in the activity rhythm of capuchins and Rhipidomys rodents suggest these nocturnal small mammals were opportunistically hunted by the monkeys as a side-effect of the trapping procedures. The ability to search in branch holes, though, is noteworthy and did not seem to depend on the research activity at the site. There is no food scarcity at the study site, owing to human provisioning, so it is unlikely that hunger stimulated the quick learning that allowed the exploitation of this “new” prey item. These observations are evidence of the curious and opportunistic nature of Cebus cay, even though it is not known how widespread this behavior was among group members.
Acknowledgments
We are grateful to the administration and staff of Cabeceira do Prata Private Reserve for the permission to work in the area and for their logistic support. We are also grateful to Instituto de Pesquisas Cananéia (IpeC), Sociedade de Pesquisa em Vida Selvagem e Educação Ambiental (SPVS) and Fundação Neotrópica do Brasil for providing research equipment. We thank Daniel Huet, Cecília Brosig, Natacha Sobanski and Janaina Casella for fieldwork assistance, and João Oliveira and Christopher Tribe for rodent species identification. Marja Z. Milano was awarded with a Master's studentship from the Brazilian Higher Education Authority (CAPES).