Substrate optimization in nut cracking by capuchin monkeys (Cebus apella)

We conducted an experiment to examine the effect of substrate on the nut-cracking behavior of a group of semicaptive capuchin monkeys. We wanted to determine whether tufted capuchin monkeys were selective in choosing the substrate on which they pound nuts, and whether the choice of substrate affected the outcome. Eight adult females and eight juveniles were provided with nuts in the outdoor facility. We found that 1) all adult females and three young capuchins succeeded in cracking nuts; 2) they preferred the hardest substrates (concrete and stone); 3) there is a link between the substrate and the amount of time needed to crack a nut; 4) most young capuchins used various substrates, some of which were inadequate, in a haphazard manner; and 5) there are different forms of nut cracking. We conclude that adult capuchins choose the hardest substrates, and that these substrates support efficient cracking.     

Tool use in wild capuchin monkeys (Cebus albifrons trinitatis)

White-fronted capuchins were observed to use leaves as cups to retrieve water from tree cavities. On multiple occasions several individuals performed this behavior. Thus, these capuchins engage in habitual tool use, as defined by McGrew's classificatory scheme of tool using behavior. Am. J. Primatol. 46:259–261, 1998. © 1998 Wiley-Liss, Inc.     

How bearded capuchin monkeys (Sapajus libidinosus) prepare to use a stone to crack nuts

Bearded capuchin monkeys crack nuts with naturally varying stone hammers, suggesting they may tune their grips and muscular forces to each stone. If so, they might use discrete actions on a stone before lifting and striking, and they would likely use these actions more frequently when the stone is larger and/or less familiar and/or when first initiating striking. We examined the behavior of (a) four monkeys (all proficient at cracking nuts) with two larger (1 kg) and two smaller (0.5 kg) stones, (b) 12 monkeys with one 1 kg stone, and (c) one monkey during its first 100 strikes with an initially unfamiliar 1 kg stone. Bearded capuchin monkeys used three discrete actions on the stone before striking, all more often with the larger stones than the smaller stones. We infer that the first discrete action (Spin) aided the monkey in determining where to grip the stone, the second (Flip) allowed it to position the stone on the anvil ergonomically before lifting it, and the third (Preparatory Lift) readied the monkey for the strenuous lifting action. The monkey that provided 100 strikes with one initially unfamiliar stone performed fewer Spins in later strikes but performed Flip and Preparatory Lift at consistent rates. The monkeys gripped the stone with both hands along the sides to lift it, but usually moved one or both hands to the top of the stone at the zenith of the lift for the downward strike. The findings highlight two new aspects of the capuchins’ nut‐cracking: (a) Anticipatory actions with the stone before striking, especially when the stone is larger or unfamiliar, and when initiating striking and (b) shifting grips on the stone during a strike. We invite researchers to investigate if other taxa use anticipatory actions and shift their grips during percussive activity.     

Capuchin monkey (Cebus apella) grips for the use of stone tools

This research examined capuchin monkey (Cebus apella) grips for the use of throwing, nut-cracking, and cutting tools. We provided subjects with stones and apparatus that accommodated the use of stones as tools. Our subjects exhibited five grips, two of which the animals used when force was the primary consideration (power grips) and three of which the animals use when accuracy of sensory judgment and instrumentation was required (precision grips). We believe that the range of contexts in which capuchins use stone tools, combined with the ability of capuchins to employ both power and precision grips as part of their tool repertoire, indicate that Cebus apella can be used to identify grips that facilitated hominid lithic technology. Am J Phys Anthropol 103:131–135, 1997. © 1997 Wiley-Liss, Inc.     

Effects of manipulatable objects on the activity of captive capuchin monkeys (Cebus apella)

The aim of this study was to evaluate simple behavioral enrichment procedures for a captive group of tufted capuchin monkeys (Cebus apella). We examined the effects of providing a manipulatable substrate (straw) and a variety of portable objects in the monkeys' home cage. The animals were observed across three conditions in two replications: 1) No portable objects were present; 2) a set of six identical portable objects was present; and 3) a set of six varied portable objects was present. The cage floor was bare in the first replication; straw was uniformly spread on the cage floor in the second replication. An 18-month period of qualitative note taking followed completion of the initial data collection phase. The presence of straw and portable objects affected patterns of affiliation by decreasing quiet contact and close proximity. Providing additional manipulative opportunities affected both the form and frequency of object-directed activities. Object contacts were directed toward a greater variety of targets, and some objects were spontaneously used as tools. Manipulation of provided objects and use of objects as tools have become routine activities in this group of monkeys. We conclude that providing straw and portable objects in an already well equipped cage is an effective means of long-term behavioral enrichment for captive capuchin monkeys. Enabling captive capuchins to express species-typical manipulative tendencies is apparently conducive to the monkeys' optimal physical and psychological well-being as well as interesting to the human observer.     

Characteristics of hammer stones and anvils used by wild bearded capuchin monkeys (Cebus libidinosus) to crack open palm nuts

Capuchins living in Boa Vista (Piauì, Brazil) crack open hard palm nuts on hard, level surfaces (anvils) using stones (hammers) as percussive tools. This activity leaves diagnostic physical remains: distinctive shallow depressions (pits) on the surface of the anvil, cracked shells, and stone hammers on the anvil. To initiate comparison of percussive stone tool use and interpretation of the artifacts it produces across capuchins, chimpanzees, and hominins, we describe a sample of the anvils and hammer stones used by capuchin monkeys at our site. Anvils (boulders and logs) were located predominantly in the transition zone between the flat open woodland and ridges, in locations that offered some overhead coverage, and with a tree nearby, but not necessarily near palm trees. Anvils contained shallow, hemispherical pits with smooth interiors. Hammers represent a diverse assemblage of ancient rocks that are much harder than the prevailing sedimentary rock out of which they eroded. Hard stones large enough to serve as hammers were more abundant on the anvils than in the surrounding area, indicating that capuchins transport them to the anvils. Capuchins use hammers weighing on average more than 1 kg, a weight that is equivalent to 25-40% of the average body weight for adult males and females. Our findings indicate that capuchins select stones to use as hammers and transport stones and nuts to anvil sites. Wild capuchins provide a new reference point for interpreting early percussive stone tool use in hominins, and a point of comparison with chimpanzees cracking nuts.     

Throwing behavior and mass distribution of stone selection in tufted capuchin monkeys (Cebus apella)

Cannell [Journal of Archaeological Science 29:335-339, 2002] argued that sex-based differences among humans in terms of the mass of chosen throwing stones could be used to infer body mass and patterns of sexual dimorphism in early hominids from Olduvai and Koobi Fora by examining the mass distributions of unaltered stone tools at those sites. We examined this hypothesis in tufted capuchin monkeys using a comparative approach, by investigating the relationships among body mass, sex, stone weight preference, and accuracy in a throwing task. The subject sample consisted of nine monkeys trained to perform an aimed-throwing task in which a food reward could be obtained by throwing a stone into a bucket. We found that 1) the subjects showed a strong mean stone mass preference; 2) the females chose heavier stones than the males, in terms of absolute mean selected stone mass and selected stone mass relative to body mass; 3) subjects threw more accurately when they used stones of preferred mass vs. stones of nonpreferred mass; and 4) overall, the males were more accurate in the throwing task than the females. We conclude that capuchins are highly selective when choosing throwing stones, and that this confers an advantage for throwing accuracy. Our results indicate that the sexually dimorphic pattern in stone mass preference observed among humans does not generalize to Cebus apella. We suggest that researchers examining this pattern in humans in an attempt to explain early hominid patterns of dimorphism and behavior should take into account not only stone weight preference, but also its adaptive advantage.     

Mark tests for mirror self-recognition in capuchin monkeys (Cebus apella) trained to touch marks

In Experiment 1, three capuchin monkeys (Cebus apella) were exposed to a mirror in their home cage for 3 days and then given food treats for touching orange marks located on the surface of an experimental chamber. Following training, a mirror was added to the chamber to see if the monkeys would use it to guide non-reinforced contacts with an orange mark on their foreheads that was only visible as a mirror reflection (mark test). Two monkeys touched the head-mark more often with the mirror present than absent, but no mark touches were emitted while looking at the mirror. In Experiment 2, the monkeys were rewarded for touching orange marks on their bodies that were directly visible, followed by another head-mark test. Again, two monkeys touched the mark more often with the mirror present than absent, but these contacts were not emitted while looking at the mirror. Since facing the mirror while mark touching was not required for reinforcement during training, Experiment 3 further tested the possibility that increased mark touching in the presence of the mirror during Experiments 1 and 2 was the result of a memorial process. For this, a final, novel mark test was conducted using an orange mark on the neck that was only visible as a reflection (Experiment 3). No monkeys passed this test. These are the first mark tests given to capuchin monkeys. The results are consistent with the finding that no monkey species is capable of spontaneous mirror self-recognition. The implications of sequential training and mark testing for comparative evaluations of mirror self-recognition capacity are discussed.     

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 (Piauí, 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. © 2008 Wiley‐Liss, Inc.     

Attending to the outcome of others: disadvantageous inequity aversion in male capuchin monkeys (Cebus apella)

Brosnan and de Waal [Nature 425:297-299, 2003] reported that capuchin monkeys responded negatively to unequal reward distributions between themselves and another individual when comparing their own rewards with that of their partner. It was suggested that social emotions provided the underlying motivation for such behavior and that this inequity aversion is specific to the social domain. However, alternative hypotheses such as the "frustration effect" or the "food expectation hypothesis" may provide more parsimonious explanations for Brosnan and de Waal's [Nature 425:297-299] results, while others have argued that these findings are not congruent with the Fehr-Schmidt inequity aversion model cited by the authors. The claim that inequity aversion behavior is specific to the social domain has also been questioned, as primates also develop expectations about rewards in the absence of partners, and react negatively when those expectations are violated. In this study, a modified Dictator game was used to investigate whether capuchins would exhibit either disadvantageous inequity aversion behavior or reference-dependent expectancy violation in social and nonsocial conditions, respectively. When given the choice between an equitable and an inequitable outcome, the subjects showed disadvantageous inequity aversion behavior, choosing the equitable outcome significantly more in the social condition. In the nonsocial condition, however, subjects did not show negative expectancy violation resulting from the formation of reference-dependent expectations, choosing the equitable outcome at chance levels. These results suggest that capuchins attend to differential payoffs and that they are averse to inequity, which is disadvantageous to themselves.     

Optional tool use: The case of wild bearded capuchins (Sapajus libidinosus) cracking cashew nuts by biting or by using percussors

Tool use in humans can be optional, that is, the same person can use different tools or no tool to achieve a given goal. Strategies to reach the same goal may differ across individuals and cultures and at the intra‐individual level. This is the first experimental study at the intra‐individual level on the optional use of a tool in wild nonhuman primates. We investigated optional tool use by wild bearded capuchins (Sapajus libidinosus) of Fazenda Boa Vista (FBV; Piauí, Brazil). These monkeys habitually succeed in cracking open the mesocarp of dry cashew nuts (Anacardium spp.) by pounding them with stones and/or by biting. We assessed whether availability of a stone and resistance of the nut affected capuchins' choice to pound or to bite the nuts and their rates of success. Sixteen capuchins (1–16 years) received small and large dry cashew nuts by an anvil together with a stone (Stone condition) or without a stone (No‐Stone condition). In the Stone conditions, subjects used it to crack the nut in 89.1% (large nuts) and 90.1% (small nut) of the trials. Nut size significantly affected the number of strikes used to open it. Availability of the stone significantly increased the average percent of success. In the No‐Stone conditions, monkeys searched for and used other percussors to crack the nuts in 54% of trials. In all conditions, age affects percentage of success and number of strikes to reach success. We argue that exclusive use of stones in other sites may be due to the higher abundance of stones at these sites compared with FBV. Since capuchins opened cashews with a tool 1–2 years earlier than they succeed at cracking more resistant palm nuts, we suggest that success at opening cashew nuts with percussors may support the monkeys' persistent efforts to crack palm nuts.     

Spontaneous tool use by wild capuchin monkeys (Cebus libidinosus) in the Cerrado

Among primates, only chimpanzees and orang-utans are credited with customary tool use in nature. Among monkeys, capuchins stand out with respect to the number of accounts of tool use. However, the majority of capuchin tool use observations reported in nature is anecdotal or idiosyncratic. In this report, we documented the stone pounding of dry fruits (Hymenea courbaril and Acrocomia aculeata) in two wild free-ranging groups of Cebus libidinosus in the Brasilia National Park, a preserved area representative of the Cerradobiome of Central Brazil. In 2004, we noted 2 episodes at which 4 monkeys used stones to crack open nuts. In 2005, we recorded 5 pounding episodes involving 2 different monkeys. Observations of tool use over the course of 2 consecutive years by some individuals, as well as other indirect evidence, indicate that this behaviour could be habitual in the studied groups. We propose that the probability of the emergence of the use of pounding stones as tools may be dependent on the ecological variables that influence the degree of terrestriality and extractive foraging and the complex interaction of these factors.     

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] and [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.