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.     

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 (Piauí, 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.     

Physical properties of palm fruits processed with tools by wild bearded capuchins (Cebus libidinosus)

Habitually, capuchin monkeys access encased hard foods by using their canines and premolars and/or by pounding the food on hard surfaces. Instead, the wild bearded capuchins (Cebus libidinosus) of Boa Vista (Brazil) routinely crack palm fruits with tools. We measured size, weight, structure, and peak-force-at-failure of the four palm fruit species most frequently processed with tools by wild capuchin monkeys living in Boa Vista. Moreover, for each nut species we identify whether peak-force-at-failure was consistently associated with greater weight/volume, endocarp thickness, and structural complexity. The goals of this study were (a) to investigate whether these palm fruits are difficult, or impossible, to access other than with tools and (b) to collect data on the physical properties of palm fruits that are comparable to those available for the nuts cracked open with tools by wild chimpanzees. Results showed that the four nut species differ in terms of peak-force-at-failure and that peak-force-at-failure is positively associated with greater weight (and consequently volume) and apparently with structural complexity (i.e. more kernels and thus more partitions); finally for three out of four nut species shell thickness is also positively associated with greater volume. The finding that the nuts exploited by capuchins with tools have very high resistance values support the idea that tool use is indeed mandatory to crack them open. Finally, the peak-force-at-failure of the piassava nuts is similar to that reported for the very tough panda nuts cracked open by wild chimpanzees; this highlights the ecological importance of tool use for exploiting high resistance foods in this capuchin species.     

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.     

Transport of Functionally Appropriate Tools by Capuchin Monkeys (Cebus apella)

Capuchin monkeys (Cebus sp.) are notable among New World monkeys for their widespread use of tools. Like chimpanzees, they use both hammer tools and insertion tools in the wild to acquire food that would be unobtainable otherwise. Recent evidence indicates that capuchins transport stones to anvil sites and use the most functionally efficient stones to crack nuts. We further investigated capuchins’ assessment of functionality by testing their ability to select a tool that was appropriate for two different tool‐use tasks: A stone for a hammer task and a stick for an insertion task. To select the appropriate tools, the monkeys investigated a baited tool‐use apparatus (insertion or hammer), traveled to a location in their enclosure where they could no longer see the apparatus, made a selection between two tools (stick or stone), and then could transport the tool back to the apparatus to obtain a walnut. We incorporated tool transport and the lack of a visual cue into the design to assess willingness to transport the tools and the monkeys’ memory for the proper tool. Six brown capuchins (Cebus apella) were first trained to select and use the appropriate tool for each apparatus. Four animals completed training and were then tested by allowing them to view a baited apparatus and then travel to a location 8 m distant where they could select a tool while out of view of the apparatus. All four monkeys chose the correct tool significantly more than expected and transported the tools back to the apparatus. Results confirm capuchins’ propensity for transporting tools, demonstrate their capacity to select the functionally appropriate tool for two different tool‐use tasks, and indicate that they can retain the memory of the correct choice during a travel time of several seconds.     

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.     

The physical characteristics and usage patterns of stone axe and pounding hammers used by long‐tailed macaques in the Andaman Sea region of Thailand

Stone hammering in natural conditions has been extensively investigated in chimpanzees and bearded capuchins. In contrast, knowledge of stone tool use in wild Old World monkeys has been limited to anecdotal reports, despite having known for over 120 years that Macaca fascicularis aurea use stone tools to process shelled foods from intertidal zones on islands in the Andaman Sea. Our report is the first scientific investigation to look at the stone tools used by these macaques. We observed they were skilled tool users and used stone tools daily. They selected tools with differing qualities for differing food items, and appeared to use at least two types of stone tools. Pounding hammers were used to crush shellfish and nuts on anvils and axe hammers were used to pick or chip at oysters attached to boulders or trees. We found significant physical differences between these two tools. Tools at oyster beds were smaller and exhibited scarring patterns focused more often on the points, whereas tools found at anvils were larger and showed more scarring on the broader surfaces. We also observed grip differences between the two tool types. Lastly, macaques struck targets with axe hammers more rapidly and over a wider range of motion than with pounding hammers. Both our behavioral and lithic data support that axe hammers might be used with greater control and precision than pounding hammers. Hand‐sized axe hammers were used for controlled chipping to crack attached oysters, and larger pounding hammers were used to crush nuts and unattached shellfish on anvils. In addition to stones, they also used hand‐sized auger shells (Turritella attenuata) as picks to axe attached oysters. Pound hammering appears similar to the stone tools used by chimpanzees and capuchins, but axe hammering has not yet been documented in other nonhuman primates in natural conditions. Am. J. Primatol. 71:594–608, 2009. © 2009 Wiley‐Liss, Inc.     

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.     

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.     

Coated nuts as an enrichment device to elicit tool use in tufted capuchins (Cebus apella)

The present paper describes a simple technique that hardens the shell of nuts and makes the use of a tool to crack them open more compelling. Walnuts were coated with a dough of sawdust and nontoxic white glue in different combinations; they were tested for hardness by using machines normally used to test different kinds of wood. Data on relative hardness for uncoated walnuts and walnuts coated with dough of two different combinations are presented. The coated walnuts were significantly harder to break than the uncoated ones, whereas no significant difference was found when comparing the hardness of two types of coated walnuts. Furthermore, observations on a captive group of tufted capuchins (Cebus apella) are described. The monkeys needed significantly more time to break open the coated walnuts. Early results show that coated walnuts may favor acquistion of tool use skills in a juvenile capuchin.     

Use of a tool-set by capuchin monkeys (Cebus apella)

The purpose of this study was to examine the use of a tool-set by capuchin monkeys (Cebus apella). Capuchins were presented with an apparatus designed to accommodate the use of pounding tools to crack walnuts and the use of probing tools to loosen and extract the inner meat. Three capuchins used stones and sticks sequentially for these purposes. The capuchins' behavior was similar in form and function to behavior that has been reported for chimpanzees in analogous situations. These results provide further evidence of the extensive tool-using capabilities of capuchin monkeys and are consistent with a hypothesis of cross-species continuity in the skillful use of tools by primates.     

Wild capuchin monkeys (Cebus libidinosus) use anvils and stone pounding tools

We conducted an exploratory investigation in an area where nut-cracking by wild capuchin monkeys is common knowledge among local residents. In addition to observing male and female capuchin monkeys using stones to pound open nuts on stone "anvils," we surveyed the surrounding area and found physical evidence that monkeys cracked nuts on rock outcrops, boulders, and logs (collectively termed anvils). Anvils, which were identified by numerous shallow depressions on the upper surface, the presence of palm shells and debris, and the presence of loose stones of an appropriate size to pound nuts, were present even on the tops of mesas. The stones used to crack nuts can weigh >1 kg, and are remarkably heavy for monkeys that weigh <4 kg. The abundance of shell remains and depressions in the anvil surface at numerous anvil sites indicate that nut-cracking activity is common and long-enduring. Many of the stones found on anvils (presumably used to pound nuts) are river pebbles that are not present in the local area we surveyed (except on or near the anvils); therefore, we surmise that they were transported to the anvil sites. Ecologically and behaviorally, nut-cracking by capuchins appears to have strong parallels to nut-cracking by wild chimpanzees. The presence of abundant anvil sites, limited alternative food resources, abundance of palms, and the habit of the palms in this region to produce fruit at ground level all likely contribute to the monkeys' routine exploitation of palm nuts via cracking them with stones. This discovery provides a new reference point for discussions regarding the evolution of tool use and material culture in primates. Routine tool use to exploit keystone food resources is not restricted to living great apes and ancestral hominids.     

Adult and juvenile bearded capuchin monkeys handle stone hammers differently during nut-cracking

Wild bearded capuchin monkeys (Sapajus libidinosus) habitually use stone hammers to crack open palm nuts and seeds on anvils. This activity requires strength, balance, and precise movement of a large stone with respect to the item placed on an anvil. We explored how well young monkeys cope with these challenges by examining their behavior and the behavior of adults while they cracked palm nuts using a stone. Using video records, we compared actions of six juvenile (2–5 years) and six adult (7+ years) wild monkeys during their first 20 strikes with one unfamiliar ellipsoid, quartzite stone (540 g), and the outcomes of these strikes. Compared with adults, juveniles cracked fewer nuts, performed a more diverse set of exploratory actions, and less frequently placed one or both hands on top of the stone on the downward motion. Adults and juveniles displayed similar low frequencies of striking with a slanted trajectory, missing the nut, and losing control over the nut or stone after striking. These findings indicate that young monkeys control the trajectory of a stone adequately but that is not sufficient to crack nuts as effectively as adults do. Compared with juveniles, adults more quickly perceive how to grip the stone efficiently, and they are able to adjust their grip dynamically during the strike. Young monkeys develop expertise in the latter aspects of cracking nuts over the course of several years of regular practice, indicating that perceptual learning about these aspects of percussion occurs slowly. Juvenile and adult humans learning to use stones to crack nuts also master these features of cracking nuts very slowly.     

Wild Bearded Capuchins Process Cashew Nuts Without Contacting Caustic Compounds

Complex and flexible food processing was a key element for the evolutionary success of hominins, enlarging the range of exploitable foods while enabling occupation of new habitats. Only a few primate species crack open encased food by using percussive tools and/or avoid physical contact with irritant compounds by removing the structures containing them. We describe, for the first time, how a population of bearded capuchin monkeys (Sapajus libidinosus) accesses the nutritious kernel of cashew nuts avoiding the caustic chemicals protecting it. Two processing strategies, namely rubbing/piercing and stone tool use, are used according to maturity of the nuts. The frequency of cashew nuts processing increases with capuchin age, and the same set of processing strategies appears to be absent in other capuchin populations, making cashew nuts processing an excellent candidate for social transmission. Am. J. Primatol. 75:387‐393, 2013. © 2013 Wiley Periodicals, Inc.     

Wild Bearded Capuchin Monkeys (Sapajus libidinosus) Strategically Place Nuts in a Stable Position during Nut-Cracking

Humans can use hand tools smoothly and effectively in varying circumstances; in other words, skillfully. A few other species of primates crack encased foods using hammer tools and anvils. Are they skilled? Positioning the food on the anvil so that it does not fall off when struck is a component of skilled cracking. We discovered that bearded capuchin monkeys deliberately place palm nuts in a relatively stable position on the anvil before striking them. In the first experiment, we marked the meridians of palm nuts where they stopped when rolled on a flat surface (“Stop meridian”). We videotaped monkeys as they cracked these nuts on an anvil. In playback we coded the position of the Stop meridian prior to each strike. Monkeys typically knocked the nuts on the anvil a few times before releasing them in a pit. They positioned the nuts so that the Stop meridian was within 30 degrees of vertical with respect to gravity more often than expected, and the nuts rarely moved after the monkeys released them. In the second experiment, 14 blindfolded people (7 men) asked to position marked nuts on an anvil as if to crack them reliably placed them with the Stop meridian in the same position as the monkeys did. In the third experiment, two people judged that palm nuts are most bilaterally symmetric along a meridian on, or close to, the Stop meridian. Thus the monkeys reliably placed the more symmetrical side of the nuts against the side of the pit, and the nuts reliably remained stationary when released. Monkeys apparently used information gained from knocking the nut to achieve this position. Thus, monkeys place the nuts skillfully, strategically managing the fit between the variable nuts and pits in the anvil, and skilled placement depends upon information generated by manual action.     

The use of probing tools by tufted capuchins (cebus apella): evidence for increased right-hand preference with age

We examined hand preference in the use of tools by tufted capuchins (Cebus apella). We presented a colony of monkeys with an enclosed container designed to accommodate the use of probing tools. Over an 8-month period, 13 monkeys used probes to extract sweet syrup from the narrow opening of the apparatus. Five monkeys exhibited bias toward use of their right hand and eight monkeys exhibited bias toward use of their left hand. Adult monkeys exhibited a greater percentage of right-hand preferent probing sequences than did juveniles. These results are consistent with hypotheses that in tasks that involve the use of tools, nonhuman primates exhibit strong lateral asymmetries at the individual level, a moderate left-hand bias at the population level, and increased bias with age toward use of the right hand.     

Ant-Gathering with Tools by Captive Tufted Capuchins (Cebus apella)

We examined ant-gathering with tools by captive tufted capuchins (Cebus apella) via two experiments. In Experiment 1, we provided groups of subjects with sticks and small branches and an apparatus that accommodated the use of tools to gather ants. In Experiment 2, we sealed the apparatus with acetate and provided the same subjects with sticks and stones. Seven of 14 subjects used sticks and leaves as probes to extract ants from the apparatus. Six of them modified probes by detaching sticks from larger branches, breaking sticks into two or more pieces, and subtracting leaves and bark. Three subjects later used a stone and stick tool-set to penetrate acetate barriers and to extract ants. These results demonstrate the use of tools by Cebus to capture moving prey and are consistent with the idea that sensorimotor skills associated with the production and use of tools in primates evolved convergently in capuchins and great apes.     

The stone tools of capuchins (Cebus apella)

We examined the production of stone took by capuchins (Cebus apella). Eleven subjects used five reduction techniques to produce 346 stone tools (48 cores and 298 flakes). They produced a sharp edge on 83% of the cores and largest flakes. Three monkeys later used a sample of these objects as cutting tools. These results demonstrate that monkeys produce lithic tools analogous to those produced by Oldowan hominids.     

Hand preference in capuchin monkeys varies with age

The purpose of this research was to examine the influence of age on hand preference in capuchin monkeys (Cebus apella). Twenty-two capuchins, aged 6 months to 30 years, were presented with a task that involved reaching for food and a task that involved using sponging tools to absorb juice. Adults exhibited a greater percentage of right-handed actions in each task than did immature subjects. Adults also exhibited a stronger lateral bias than did immature subjects in the sponging task. These results are consistent with hypotheses: a) adult capuchin monkeys are biased toward use of their right hand for reaching; b) adult capuchins exhibit a greater incidence of right-hand preference than do immature capuchins; and c) primates exhibit age-related differences in the strength and direction of hand preference in tasks that involve the use of tools.     

Semifree-ranging Tufted Capuchins (Cebus apella) Spontaneously Use Tools to Crack Open Nuts

Naturalistic studies on tool use by nonhuman primates have focused almost exclusively on Old World monkeys or hominoids. We studied the cracking of Syagrus nuts with the aid of stones by a group of semifree-ranging capuchins living in a reforested area (Tietê Ecological Park, São Paulo, Brazil). Our data are from direct observation and from mapping nut-cracking site utilization. All adults, subadults and juveniles (plus one infant) crack nuts, but individual differences in frequency and proficiency are marked. Juveniles do most of the nut-cracking, but adults are, on average, more efficient; the frequency of inept stone manipulation decreases with age. About 10% of the nut-cracking episodes were watched by other individuals—mostly infants and juveniles, suggesting a role for observational learning, even if restricted to stimulus enhancement.