Introduction

Neotropical primates affect plant population through mutualistic intetactions, such as seed dispetsal, and antagonist interactions such as seed predation and hetbivoty (Peres, 1993; Russo and Augspurger, 2004; Mourthé et al., 2008). Primates killing trees through hetbivoty is rarely documented (Rocha, 2000; Santos et al., 2007). The genus Cebus (Erxleben, 1777) is considered as having the widest diet plasticity among neotropical primates, eating leaves, seeds, fruits, invertebrates and even vertebrates (Fedigan, 1990; Galetti and Pedroni, 1994; Susan and Rose, 1994; Rose, 1996; Ludwig et al., 2005; Carretero-Pinzón et al., 2008; Freitas et al., 2008). In this paper, we documented the predation of two palm species through the consumption of palm heart (apical meristem) by black-capuchin monkey (Cebus nigritus Goldfuss, 1809).

Materials and methods

Our observations were carried out between June 2009 and June 2010 in “Carlos Botelho” State Park (CBSP) (24°06′ and 24°14′S; 47°47′ and 48°07′W, in São Paulo State, Brazil. The CBSP has an area of 37,644 ha of Atlantic Forest, and it is located in the Forest Continuum of Paranapiacaba massif. The annual average temperature vatied from 15 to 19 °C, and the annual precipitation varied from 1700 to 2400 mm (Instituto Florestal, 2008). The density of black-capuchin monkeys in this site is estimated at 10.5 (± 2.4 SE) individuals/km², and the average group size is 5.16 (±0.55 SE) individuals (Galetti et al., unpub. data).

The records of palm heart predation (directly and indirectly) were taken during line transects of mammal survey (430 km, approach 500 hours) and during the displacements to line transects in the forest (about 200 field hours). Despite that the C. nigritus groups were not accompanied directly, the animals are relatively habituated to observers. The line transects surveys were carried monthly (10–15 days per month), when we encounter predation events, ad libitum observations were made (with binoculars or naked eye), each predation event was recorded by a single observer. We sampled adult trees through randomized 15 0.04-ha plots, and juvenile trees through 15 0.01-ha plots to estimate the capuchin-monkey palm ptedation (sampling tree adapted from Durigan, 2003). Chi-square analysis was used to estimate differences in predation intensity between seasons.

Results

We observed capuchin-monkeys preying upon palm hearts of Euterpe edulis Mart. in 14 occasions, being 12 times in the Winter (May–August), once in the Summet (November–February), and once in the Autumn (February–May). We recorded from one to four capuchinmonkeys (sub-adult and adult) feeding simultaneously on apical meristem, but each animal on a different palm. The group size in these events varied from 3 to 12 blackcapuchin monkeys. Capuchin monkeys spend between 10 to 40 minutes (mean 25 ± 4 SE) to open the palm heart, varying principally with palm diameter. Initially, the monkeys bite the outer leaves, forcing them down using both hands, remaining supported with tail and posterior members on the palm stipe, then they repeat this process until liberate the apex of most leaves. After that, the animals bite the apex basis, to release it from the stipe, and consumed the apical metistem on other tree.

Figure 1.

A) Remains of consumed apical meristem by C. nigritus in CBSP. B) Recently withdrawn leaves of E. edulis on the ground.

We found other 44 E. edulis killed by capuchins along the forest trails, of which 38 palms were killed in the Winter, four in the Summet, and two in the Autumn. The presence of recently signals permitted the identification of predation period (recently withdrawn leaves on the ground, recently destroyed apices and remains of consumed meristems; Fig. 1A and 1B). Other 12 palms were too old to determine the season of the predation (resting only the old destroyed apices). Considering direct and indirect observations of palms predation (only events where was possible determining the period of predation), the consumption of E. edulis differed significantly between seasons (χ² = 73.0, df = 2, p < 0.001), being 10 times higher in the Winter than Summer, and 18 times greater than in the Autumn. The E. edulis palms killed had diameter at breast height from 8.6 to 15.4 cm (mean 12.8 ± 0.55 SE) and height from 7 to 20 m (mean 12.2 ± 0.94 SE). E. edulis is the most abundant arboreal plant in the study area, with a mean density of 93.3 (± 22.8 SE) adults/ha and 706.6 (± 90.7 SE) juveniles/ha. We estimated E. edulis adult mortality by capuchin monkeys at 1.7 (± 1.6 SE) individuals/ha per year (1.8 % of adult population).

Moreover, for the first time, we observed the predation of palm heart of Geonoma gamiova Barb. Rodr., an understory palm species, with height up to 4 m. Two adults G. gamiova were upon preyed by two adult capuchin monkeys (in the Winter). The process is similar to E. edulis, but beyond the animals supported on the palm, they supported in near lianas, taking for predation 8 minutes for a palm and 9 minutes for other.

Discussion

The distribution of E. edulis and C. nigritus overlaps in most part of their occurrence in the Brazilian Atlantic Forest (Vilanova et al., 2005; Herderson, 2000) (Fig. 2A). But, the palm heart predation by capuchin monkeys has been reported in a few places (Fig. 2B). In others areas we have worked, as the Iguaçu National Park (Araucaria Forest and Semidecidual Atlantic Forest, 185,262 ha continuous area, Paraná state, Brazil) and Semidecidual Atlantic Forest fragments in São Paulo state (“Mata São José” and “Mata Santa Genebra”, both approximately 250 ha), this behavior or predation signals were never recorded. It is possible that the use of this resource may be related to the group cultural inheritance, such as tool use and food-processing (Antinucci and Visalberghi, 1986; Rocha et al., 1998; Fragaszy et al., 2004; O'Malley and Fedigan, 2005; Canale et al., 2009). The group cultural inheritance in Cebus species, as well as other primate species, involves social learning, when the animals observe and interact with other group members, acquiring behaviors (Panger et al., 2002; Dindo et al., 2008; Dindo et al., 2009). The removal of the apical meristem demands dexterity and physical effort, being not accomplished by all members of a group, commonly this is done by some adults and sub-adults, and is observed for young animals.

Except humans, C. nigritus seems to be one of the only vertebrate able to prey upon apical meristem of adults E. edulis, since white-lipped peccaries (Tayassu pecari Link, 1795) prey upon apical meristem of saplings (F. Rocha-Mendes unp. data), and one of the few primates killing an atboreal plant (see Santos et al., 2007; Rocha, 2000). E. edulis is a palm with single stipe (differently of Euterpe oleracea), and removal of apical meristem leads to the death of individual. In forest fragments the main cause of mortality of E. edulis and Geonoma brevispetha (adult and juvenile palms) is the impact of meristem ptedation by black-capuchin monkeys (Souza and Martins, 2006; Santos et al., 2007; Portela, 2008; Portela et al., 2010). In areas where this behavior occuts, the capuchin monkeys may be helping to modeling the forest structure, similar to observed for ungulates (Silman et al., 2003; Wyatt and Silman, 2004; Beck, 2007). The palm heart predation by capuchins may have consequences for other species, especially birds, rodents and ungulates that depend on E. edulis fruits during the Winter (Galetti et al., 1999; Mikich, 2002). Nevertheless, this impact is much smaller than the one caused by human extraction, which may extirpate locally entire adult populations, being the higher threat to conservation of E. edulis (Galetti and Aleixo, 1998; Galetti and Fernadez, 1998; Pizo and Vieira, 2004).

Figure 2.

A) Distribution of Cebus nigritus (triangles) and Euterpe edulis (circles) in Brazil (adapted from Vilanova et al., 2005 and Herderson, 2000); B) Areas with records of apical meristem predation of E. edulis by C. nigritus: 1 -Poços das Antas Biological Reserve, fragment (Portela, 2008; Portela et al., 2010); 2 - Caetetus Ecological Station, fragment (R. Lázara pers. com.); 3 - CBSP, continuous (this paper, Taira, 2007); 4 -Intervales State Park, continuous (Zipparro and Galetti pers. ob.); 5 -Juréia-Itatins Ecological Station , continuous (P. Rubim pers. com.); 6 - “Mata” Doralice, fragment (Ludwig et al., 2005); 7 -Vila Rica do Espírito Santo State Park, fragment (Santos et al., 2007).

Taira (2007) suggests that the consumption of palm heart in the Winter is an alternative source to insect scarcity, but not to fruit scarcity, which also occurs in the Winter at CBSP (Nakai, 2007). On the other hand, several papers concerning the diet of C. nigritus and congeners reported the use of alternative food resource in period of scarcity of fruits which normally constitute the main part of Cebus diet (Galetti and Pedroni, 1994; Peres, 1994; Freitas et al., 2008). Therefore, we suggest that palm heart of E. edulis and, at a lesser extent, of G. gamiova, might be considered as a fallback food of C. nigritus. Indeed, fallback foods are defined as “foods consumed during seasons when preferred foods are unavailable” (Altman, 1998) or as “foods whose use is negatively correlated with the availability of preferred foods” (Marshall and Wrangham, 2007; reviewed in Lambert, 2009). E. edulis is known as a keystone-species, providing fruits and seeds for several animal species during the time of greatest shortage (Galetti et al., 1999; Mikich, 2002). The consumption of meristem apical by C. nigritus, especially in the Winter, highlights another aspect of importance of this palm.