Agricultural crops in the diet of bearded capuchin monkeys, Cebus libidinosus Spix (Primates: Cebidae), in forest fragments in southeast Brazil

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)

How wild bearded capuchin monkeys select stones and nuts to minimize the number of strikes per nut cracked

Wild bearded capuchin monkeys, Cebus libidinosus, use stone tools to crack palm nuts to obtain the kernel. In five experiments, we gave 10 monkeys from one wild group of bearded capuchins a choice of two nuts differing in resistance and size and/or two manufactured stones of the same shape, volume and composition but different mass. Monkeys consistently selected the nut that was easier to crack and the heavier stone. When choosing between two stones differing in mass by a ratio of 1.3:1, monkeys frequently touched the stones or tapped them with their fingers or with a nut. They showed these behaviours more frequently before making their first selection of a stone than afterward. These results suggest that capuchins discriminate between nuts and between stones, selecting materials that allow them to crack nuts with fewer strikes, and generate exploratory behaviours to discriminate stones of varying mass. In the final experiment, humans effectively discriminated the mass of stones using the same tapping and handling behaviours as capuchins. Capuchins explore objects in ways that allow them to perceive invariant properties (e.g. mass) of objects, enabling selection of objects for specific uses. We predict that species that use tools will generate behaviours that reveal invariant properties of objects such as mass; species that do not use tools are less likely to explore objects in this way. The precision with which individuals can judge invariant properties may differ considerably, and this also should predict prevalence of tool use across species. (C) 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Bearded capuchin monkeys` and a human`s efficiency at cracking palm nuts with stone tools: field experiments

Wild bearded capuchins, Cebus libidinosus, in Fazenda Boa Vista, Brazil crack tough palm nuts using hammer stones. We analysed the contribution of intrinsic factors (body weight, behaviour), size of the nuts and the anvil surface (flat or pit) to the efficiency of cracking. We provided capuchins with local palm nuts and a single hammer stone at an anvil. From video we scored the capuchins` position and actions with the nut prior to each strike, and outcomes of each strike. The most efficient capuchin opened 15 nuts per 100 strikes (6.6 strikes per nut). The least efficient capuchin that succeeded in opening a nut opened 1.32 nuts per 100 strikes (more than 75 strikes per nut). Body weight and diameter of the nut best predicted whether a capuchin would crack a nut on a given strike. All the capuchins consistently placed nuts into pits. To provide an independent analysis of the effect of placing the nut into a pit, we filmed an adult human cracking nuts on the same anvil using the same stone. The human displaced the nut on proportionally fewer strikes when he placed it into a pit rather than on a flat surface. Thus the capuchins placed the nut in a more effective location on the anvil to crack it. Nut cracking as practised by bearded capuchins is a striking example of a plastic behaviour where costs and benefits vary enormously across individuals, and where efficiency requires years to attain. (C) 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Stone tool use by adult wild bearded capuchin monkeys (Cebus libidinosus). Frequency, efficiency and tool selectivity

Chimpanzees have been the traditional referential models for investigating human evolution and stone tool use by hominins. We enlarge this comparative scenario by describing normative use of hammer stones and anvils in two wild groups of bearded capuchin monkeys (Cebus libidinosus) over one year. We found that most of the individuals habitually use stones and anvils to crack nuts and other encased food items. Further, we found that in adults (1) males use stone tools more frequently than females, (2) males crack high resistance nuts more frequently than females, (3) efficiency at opening a food by percussive tool use varies according to the resistance of the encased food, (4) heavier individuals are more efficient at cracking high resistant nuts than smaller individuals, and (5) to crack open encased foods, both sexes select hammer stones on the basis of material and weight. These findings confirm and extend previous experimental evidence concerning tool selectivity in wild capuchin monkeys (Visalberghi et al., 2009b; Fragaszy et al., 2010b). Male capuchins use tools more frequently than females and body mass is the best predictor of efficiency, but the sexes do not differ in terms of efficiency. We argue that the contrasting pattern of sex differences in capuchins compared with chimpanzees, in which females use tools more frequently and more skillfully than males, may have arisen from the degree of sexual dimorphism in body size of the two species, which is larger in capuchins than in chimpanzees. Our findings show the importance of taking sex and body mass into account as separate variables to assess their role in tool use. (C) 2011 Elsevier Ltd. All rights reserved.

The Enhanced Tool-Kit of Two Groups of Wild Bearded Capuchin Monkeys in the Caatinga: Tool Making, Associative Use, and Secondary Tools

The use of stones to crack open encapsulated fruit is widespread among wild bearded capuchin monkeys (Cebus libidinosus) inhabiting savanna-like environments. Some populations in Serra da Capivara National Park (Piaui, Brazil), though, exhibit a seemingly broader toolkit, using wooden sticks as probes, and employing stone tools for a variety of purposes. Over the course of 701.5 hr of visual contact of two wild capuchin groups we recorded 677 tool use episodes. Five hundred and seventeen of these involved the use of stones, and 160 involved the use of sticks (or other plant parts) as probes to access water, arthropods, or the contents of insects` nests. Stones were mostly used as ""hammers""-not only to open fruit or seeds, or smash other food items, but also to break dead wood, conglomerate rock, or cement in search of arthropods, to dislodge bigger stones, and to pulverize embedded quartz pebbles (licking, sniffing, or rubbing the body with the powder produced). Stones also were used in a ""hammer-like"" fashion to loosen the soil for digging out roots and arthropods, and sometimes as ""hoes"" to pull the loosened soil. In a few cases, we observed the re-utilization of stone tools for different purposes (N = 3), or the combined use of two tools-stones and sticks (N = 4) or two stones (N = 5), as sequential or associative tools. On three occasions, the monkeys used smaller stones to loosen bigger quartz pebbles embedded in conglomerate rock, which were subsequently used as tools. These could be considered the first reports of secondary tool use by wild capuchin monkeys. Am. J. Primatol. 71:242-251, 2009. (c) 2008 Wiley-Liss, Inc.

Selection of Effective Stone Tools by Wild Bearded Capuchin Monkeys

Appreciation of objects` affordances and planning is a hallmark of human technology. Archeological evidence suggests that Pliocene hominins selected raw material for tool making [1, 2]. Stone pounding has been considered a precursor to tool making [3, 4], and tool use by living primates provides insight into the origins of material selection by human ancestors. No study has experimentally investigated selectivity of stone tools in wild animals, although chimpanzees appear to select stones according to properties of different nut species [5, 6]. We recently discovered that wild capuchins with terrestrial habits [7] use hammers to crack open nuts on anvils [8-10]. As for chimpanzees, examination of anvil sites suggests stone selectivity [11], but indirect evidence cannot prove it. Here, we demonstrate that capuchins, which last shared a common ancestor with humans 35 million years ago, faced with stones differing in functional features (friability and weight) choose, transport, and use the effective stone to crack nuts. Moreover, when weight cannot be judged by visual attributes, capuchins act to gain information to guide their selection. Thus, planning actions and intentional selection of tools is within the ken of monkeys and similar to the tool activities of hominins and apes.

Wild bearded capuchin monkeys (Cebus libidinosus) place nuts in anvils selectively

Are wild bearded capuchin monkeys selective about where they place nuts on anvils, specifically the anvil pits, during nut cracking? In the present study, we examined (1) whether capuchins` preferences for particular pits are influenced by the effectiveness of the pit in cracking the nut and/or by the stability of the nut during striking, (2) how capuchins detect the affordances of novel pits and (3) the influence of social context on their selections. Anvil pits varied in horizontal dimension (small, medium and large) in experiment 1 and in depth (shallow, medium and deep) in experiment 2. In both experiments, three different pits were simultaneously presented, each on one anvil. We coded the capuchins` actions with the nut in each pit, and recorded the outcome of each strike. In both experiments, capuchins preferred the most effective pit, but not the most stabilizing pit, based on the number of first strikes, total strikes and nuts cracked. Their choice also reflected where the preceding individual had last struck. The capuchins explored the pits indirectly, placing nuts in them and striking nuts with a stone. The preference for pits was weaker than the preference for nuts and stones shown previously with the same monkeys. Our findings suggest that detecting affordances of pits through indirect action is less precise than through direct action, and that social context may also influence selection. We show that field experiments can demonstrate embodied cognition in species-typical activities in natural environments. (C) 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Stone tool use in wild bearded capuchin monkeys, Cebus libidinosus. Is it a strategy to overcome food scarcity?

To determine whether tool use varied in relation to food availability in bearded capuchin monkeys, we recorded anvil and stone hammer use in two sympatric wild groups, one of which was provisioned daily, and assessed climatic variables and availability of fruits, invertebrates and palm nuts. Capuchins used tools to crack open encased fruits, mostly palm nuts, throughout the year. Significant differences between wet and dry seasons were found in rainfall, abundance of invertebrates and palm nuts, but not in fruit abundance. Catule nuts were more abundant in the dry season. We tested the predictions of the necessity hypothesis (according to which tool use is maintained by sustenance needs during resource scarcity) and of the opportunity hypothesis (according to which tool use is maintained by repeated exposure to appropriate ecological conditions, such as preferred food resources necessitating the use of tools). Our findings support only the opportunity hypothesis. The rate of tool use was not affected by provisioning, and the monthly rate of tool use was not correlated with the availability of fruits and invertebrates. Conversely, all capuchins cracked food items other than palm nuts (e.g. cashew nuts) when available, and adult males cracked nuts more in the dry season when catule nuts (the most common and exploited nut) are especially abundant. Hence, in our field site capuchins use tools opportunistically. (C) 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Distribution of potential suitable hammers and transport of hammer tools and nuts by wild capuchin monkeys

Selection and transport of objects to use as tools at a distant site are considered to reflect planning. Ancestral humans transported tools and tool-making materials as well as food items. Wild chimpanzees also transport selected hammer tools and nuts to anvil sites. To date, we had no other examples of selection and transport of stone tools among wild nonhuman primates. Wild bearded capuchins (Cebus libidinosus) in Boa Vista (Piaui, Brazil) routinely crack open palm nuts and other physically well-protected foods on level surfaces (anvils) using stones (hammers) as percussive tools. Here we present indirect evidence, obtained by a transect census, that stones suitable for use as hammers are rare (study 1) and behavioral evidence of hammer transport by twelve capuchins (study 2). To crack palm nuts, adults transported heavier and harder stones than to crack other less resistant food items. These findings show that wild capuchin monkeys selectively transport stones of appropriate size and hardness to use as hammers, thus exhibiting, like chimpanzees and humans, planning in tool-use activities.

Kinematics and Energetics of Nut-Cracking in Wild Capuchin Monkeys (Cebus libidinosus) in Piaui, Brazil

Wild bearded capuchins (Cebus libidinosus, quadrupedal, medium-sized monkeys) crack nuts using large stones. We examined the kinematics and energetics of the nut-cracking action of two adult males and two adult females. From a bipedal stance, the monkeys raised a heavy hammer stone (1.46 and 1.32 kg, from 33 to 77% of their body weight) to an average height of 0.33 m, 60% of body length. Then, they rapidly lowered the stone by flexing the lower extremities and the trunk until the stone contacted the nut. A hit consisting of an upward phase and a downward phase averaged 0.74 s in duration. The upward phase lasted 69% of hit duration. All subjects added discernable energy to the stone in the downward phase. The monkeys exhibited individualized kinematic strategies, similar to those of human weight lifters. Capuchins illustrate that human-like bipedal stance and large body size are unnecessary to break tough objects from a bipedal position. The phenomenon of bipedal nut-cracking by capuchins provides a new comparative reference point for discussions of percussive tool use and bipedality in primates. Am J Phys Anthropol 138:210-220, 2009. (C) 2008 Wiley-Liss, Inc.

A Comparative Assessment of Hand Preference in Captive Red Howler Monkeys, Alouatta seniculus and Yellow-Breasted Capuchin Monkeys, Sapajus xanthosternos

There are two major theories that attempt to explain hand preference in non-human primates-the `task complexity' theory and the `postural origins' theory. In the present study, we proposed a third hypothesis to explain the evolutionary origin of hand preference in non-human primates, stating that it could have evolved owing to structural and functional adaptations to feeding, which we refer to as the `niche structure' hypothesis. We attempted to explore this hypothesis by comparing hand preference across species that differ in the feeding ecology and niche structure: red howler monkeys, Alouatta seniculus and yellow-breasted capuchin monkeys, Sapajus xanthosternos. The red howler monkeys used the mouth to obtain food more frequently than the yellow-breasted capuchin monkeys. The red howler monkeys almost never reached for food presented on the opposite side of a wire mesh or inside a portable container, whereas the yellow-breasted capuchin monkeys reached for food presented in all four spatial arrangements (scattered, on the opposite side of a wire mesh, inside a suspended container, and inside a portable container). In contrast to the red howler monkeys that almost never acquired bipedal and clinging posture, the yellow-breasted capuchin monkeys acquired all five body postures (sitting, bipedal, tripedal, clinging, and hanging). Although there was no difference between the proportion of the red howler monkeys and the yellow-breasted capuchin monkeys that preferentially used one hand, the yellow-breasted capuchin monkeys exhibited an overall weaker hand preference than the red howler monkeys. Differences in hand preference diminished with the increasing complexity of the reaching-for-food tasks, i.e., the relatively more complex tasks were perceived as equally complex by both the red howler monkeys and the yellow-breasted capuchin monkeys. These findings suggest that species-specific differences in feeding ecology and niche structure can influence the perception of the complexity of the task and, consequently, hand preference.

Evaluation of dental pulp repair using low level laser therapy (688 nm and 785 nm) morphologic study in capuchin monkeys

The aim of this study was to evaluate the hypothesis that low-level laser therapy (LLLT) 688 nm and 785 nm accelerate dentin barrier formation and repair process after traumatic pulp exposure. The sample consisted of 45 premolars of capuchin monkeys (Cebus apella) with pulp exposure Class V cavities. All premolars were treated with calcium hydroxide (Ca(OH)(2)), divided in groups of 15 teeth each, and analyzed on 7(th), 25(th), and 60(th) day. Group GI - only Ca(OH)(2), GIF- laser 688 nm, and GIII - laser 785 nm. Laser beam was used in single and punctual dose with the parameters: continuous, 688 nm and 785 nm wavelength, tip`s area of 0.00785 cm(2), power 50 mW, application time 20 s, dose 255 J/cm(2), energy 2 J. Teeth were capped with Ca(OH)(2), Ca(OH)(2) cement and restored with amalgam. All groups presented pulp repair. On 25(th) day the thickness of the formed dentin barrier was different between the groups GI and GII (p < 0.05) and between groups GI and GIII (p < 0.01). On 60(th) day there was difference between GI and GIII (p < 0.01). It may be concluded that, LLLT 688 nm and 785 nm accelerated dentin barrier formation and consequently pulp repair process, with best results using infrared laser 785 nm. (c) 2009 by Astro Ltd. Published exclusively by WLLEY-VCH Verlag GmbH & Co. KGaA

Frequency of Toxoplasma gondii antibodies in tufted capuchin monkeys (Cebus apella nigritus) from an ecological station in the State of São Paulo, Brazil

A toxoplasmose é uma das zoonoses mais difundidas no mundo, causada pelo Toxoplasma gondii, um protozoário parasita intracelular obrigatório. Uma alta porcentagem de animais apresenta anticorpos específicos causados por exposição prévia, levando a uma infecção crônica. Os felídeos são os hospedeiros definitivos e outros animais homeotérmicos, incluindo os primatas, são os hospedeiros intermediários. Este estudo objetivou determinar a prevalência da infecção por T. gondii em macacos-prego (Cebus apella nigritus) de vida livre da Estação Ecológica localizada na Mata de Santa Teresa, Ribeirão Preto, SP, Brasil. Anticorpos anti-T. gondii foram pesquisados pelo método de aglutinação direta modificada (MAT) em amostras de soro de 36 macacos-prego, utilizando-se o título oito como de corte. Dos animais estudados, 3/36 (8,33%; IC95% 3,0-21,9%) apresentaram anticorpos anti-T. gondii, todos com título 32. Nenhuma diferença significativa (P>0,05) foi observada com relação ao sexo (1/3 machos e 2/3 fêmeas), e à idade (1/3 jovens e 2/3 adultos). Assim, estes resultados demonstram alta prevalência de anticorpos anti-T. gondii em primatas no estado de São Paulo.

Exposure to rabies virus in a population of free-ranging capuchin monkeys (Cebus apella nigritus) in a fragmented, environmentally protected area in southeastern Brazil

The aim of this study is to assess the frequency of rabies antibodies in free-ranging capuchin monkeys (Cebus apella nigritus) in a fragmented, environmentally protected, rural area of southeastern Brazil. Thirty-six free-ranging monkeys were tested by the rapid fluorescent focus inhibition test for detection of antibodies against rabies virus. Four individuals (11.11 %) had neutralizing antibody titers a parts per thousand yen0.25 IU/mL, demonstrating rabies virus exposure.