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.     

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.     

Stone Anvil Damage by Wild Bearded Capuchins (Sapajus libidinosus) during Pounding Tool Use: A Field Experiment

We recorded the damage that wild bearded capuchin monkeys (Sapajus libidinosus) caused to a sandstone anvil during pounding stone tool use, in an experimental setting. The anvil was undamaged when set up at the Fazenda Boa Vista (FBV) field laboratory in Piauí, Brazil, and subsequently the monkeys indirectly created a series of pits and destroyed the anvil surface by cracking palm nuts on it. We measured the size and rate of pit formation, and recorded when adult and immature monkeys removed loose material from the anvil surface. We found that new pits were formed with approximately every 10 nuts cracked, (corresponding to an average of 38 strikes with a stone tool), and that adult males were the primary initiators of new pit positions on the anvil. Whole nuts were preferentially placed within pits for cracking, and partially-broken nuts outside the established pits. Visible anvil damage was rapid, occurring within a day of the anvil''s introduction to the field laboratory. Destruction of the anvil through use has continued for three years since the experiment, resulting in both a pitted surface and a surrounding archaeological debris field that replicate features seen at natural FBV anvils.     

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.     

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.     

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.     

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.     

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.     

New data on the use of stone tools by chimpanzees in Guinea and Liberia

Two types of use of “hammers” for cracking nuts by wild-living chimpanzees have been distinguished: (1) Relatively small stones are used by the chimpanzee community at Bossou in Guinea to crack the nuts of oil palms growing on abandoned farmland, while no nuts of wild tree species are cracked. (2) Larger hammer stones (and, at some sites, wooden clubs) are used in a more sophisticated manner to crack the nuts of wild trees, but not of oil palms, in an area ranging from south-east Sierra Leone through Liberia to the south-west of the Ivory Coast. The first author (1986) has proposed that Type I has been copied by the chimpanzees, under pressure of food shortage, from the local human population. New data now indicate that, at Bossou, while habitat deterioration has continued, the number of hammer and anvil stones per utilized oil palm tree has approximately tripled in the last six years. The quantity of food obtained from oil palm nut kernels, however, amounts to only a few percent of the total diet. For the rest these apes depend to a large extent on many other agricultural products cultivated at Bossou which they are allowed freely to consume, including even cassava (manioc) roots and sweet potatoes dug by them from the ground. Some factors determining the chosen size of hammers were analyzed. Two abnormal hammers were found whose wear suggested a tentative, human-like manner of use. No evidence has been found to indicate the use of stone tools by chimpanzees in the adjoining chimpanzee-inhabited areas around the range of the Bossou community. Type II stone tool use was found, however, in a primary forest on a mountain≈13 km west of Bossou. This is especially intriguing because the site is separated by a wide belt of drier rain forest from the belt of very humid rain forest in the south where all the other known Type II sites are located. More research on the geographical distribution of the use of stone tools by chimpanzees and on the underlying ecological factors is recommended.     

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.     

Sooty mangabeys scavenge on nuts cracked by chimpanzees and red river hogs—An investigation of inter‐specific interactions around tropical nut trees

Carrion scavenging is a well‐studied phenomenon, but virtually nothing is known about scavenging on plant material, especially on remnants of cracked nuts. Just like meat, the insides of hard‐shelled nuts are high in energetic value, and both foods are difficult to acquire. In the Taï forest, chimpanzees (Pan troglodytes) and red river hogs (Potamochoerus porcus) crack nuts by using tools or strong jaws, respectively. In this study, previously collected non‐invasive camera trap data were used to investigate scavenging by sooty mangabeys (Cercocebus atys), two species of Guinea fowl (Agelestres meleagrides; Guttera verreauxi), and squirrels (Scrunidae spp.) on the nut remnants cracked by chimpanzees and red river hogs. We investigated how scavengers located nut remnants, by analyzing their visiting behavior in relation to known nut‐cracking events. Furthermore, since mangabeys are infrequently preyed upon by chimpanzees, we investigated whether they perceive an increase in predation risk when approaching nut remnants. In total, 190 nut‐cracking events were observed in four different areas of Taï National Park, Ivory Coast. We could confirm that mangabeys scavenged on the nuts cracked by chimpanzees and hogs and that this enabled them to access food source that would not be accessible otherwise. We furthermore found that mangabeys, but not the other species, were more likely to visit nut‐cracking sites after nut‐cracking activities than before, and discuss the potential strategies that the monkeys could have used to locate nut remnants. In addition, mangabeys showed elevated levels of vigilance at the chimpanzee nut‐cracking sites compared with other foraging sites, suggesting that they perceived elevated danger at these sites. Scavenging on remnants of cracked nuts is a hitherto understudied type of foraging behavior that could be widespread in nature and increases the complexity of community ecology in tropical rainforests.     

Kinematics and energetics of nut-cracking in wild capuchin monkeys (Cebus libidinosus) in Piauí, 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.     

How does stone-tool use emerge? Introduction of stones and nuts to naïve chimpanzees in captivity

Nut-cracking behavior has been reported in several communities in West Africa but not in East and Central Africa. Furthermore, even within nut-cracking communities, there are individuals who do not acquire the skill. The present study aimed to clarify the cognitive capability required for nut-cracking behavior and the process through which the the nut-cracking behavior emerges. To examine emergence, we provided three naïve adult chimpanzees with a single opportunity to observe human models. A human tester demonstrated nut-cracking behavior using a pair of stones and then supplied stones and nuts to the chimpanzee subjects. Two out of three chimpanzees proceeded to hit a nut on an anvil stone using a hammer stone, one of whom succeeded in cracking open the nuts during the first test session. The third chimpanzee failed to crack open nuts. We used four variables (object, location, body part used, and action) to describe stone/nut manipulation in order to analyze further the patterns of object manipulation exhibited by the subjects. The analysis revealed that there were three main difficulties associated with nut-cracking behavior. (1) The chimpanzee who failed at the task never showed hitting action. (2) The chimpanzee who failed at the task manipulated nuts but rarely stones. (3) The combination of three objects was not commonly observed in the three chimpanzees. We also discuss our results with reference to the effect of enculturation in captivity and the social context of learning in the wild.     

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.     

Technological Response of Wild Macaques (<Emphasis Type="Italic">Macaca fascicularis</Emphasis>) to Anthropogenic Change

Anthropogenic disturbances have a detrimental impact on the natural world; the vast expansion of palm oil monocultures is one of the most significant agricultural influences. Primates worldwide consequently have been affected by the loss of their natural ecosystems. Long-tailed macaques (Macaca fascilularis) in Southern Thailand have, however, learned to exploit oil palm nuts using stone tools. Using camera traps, we captured the stone tool behavior of one macaque group in Ao Phang-Nga National Park. Line transects placed throughout an abandoned oil palm plantation confirmed a high abundance of nut cracking sites. Long-tailed macaques previously have been observed using stone tools to harvest shellfish along the coasts of Thailand and Myanmar. The novel nut processing behavior indicates the successful transfer of existing lithic technology to a new food source. Such behavioral plasticity has been suggested to underlie cultural behavior in animals, suggesting that long-tailed macaques have potential to exhibit cultural tendencies. The use of tools to process oil palm nuts across multiple primate species allows direct comparisons between stone tool using nonhuman primates living in anthropogenic environments.     

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.     

Identification and characterization of differential gene expression in the mesocarp and kernel of oil palm nuts using suppression subtractive hybridization

Suppression subtracted hybridization (SSH) and dot blotting were used to identify differential gene expression in the mesocarp and kernel of oil palm nuts. The different types of nut tissue show differences in fatty acid anabolism and the synthesis of other important compounds. In total, 302 clones from forward SSH libraries and 238 clones from reverse SSH libraries were identified following differential screening, respectively. Among these, 120 clones from the forward SSH library and 81 clones from the reverse SSH library, showed tenfold or more differential expression levels, and were sequenced. Sequence analysis revealed that 76 clones (28 from the forward SSH library and 48 from the reverse SSH library) represent non-redundant cDNA inserts. The differential expression of 39 subset genes in the two different tissues was further confirmed by RT-PCR analysis. Functionally annotated blasting against the GenBank non-redundant protein database classified all 76 candidate genes into six categories, according to their putative functions. Interestingly, our results show that a group of significantly differentially expressed genes are involved in processes associated with oil palm nut maturation, such as the synthesis of medium-chain saturated fatty acids and phytic acid, nut development, and stress/defense responses. This study describes some relationships between gene expression and metabolic pathways in mature oil palm nuts, and contributes to our understanding of oil palm nut ESTs.     

Macaque Monkeys Can Learn Token Values from Human Models through Vicarious Reward

Monkeys can learn the symbolic meaning of tokens, and exchange them to get a reward. Monkeys can also learn the symbolic value of a token by observing conspecifics but it is not clear if they can learn passively by observing other actors, e.g., humans. To answer this question, we tested two monkeys in a token exchange paradigm in three experiments. Monkeys learned token values through observation of human models exchanging them. We used, after a phase of object familiarization, different sets of tokens. One token of each set was rewarded with a bit of apple. Other tokens had zero value (neutral tokens). Each token was presented only in one set. During the observation phase, monkeys watched the human model exchange tokens and watched them consume rewards (vicarious rewards). In the test phase, the monkeys were asked to exchange one of the tokens for food reward. Sets of three tokens were used in the first experiment and sets of two tokens were used in the second and third experiments. The valuable token was presented with different probabilities in the observation phase during the first and second experiments in which the monkeys exchanged the valuable token more frequently than any of the neutral tokens. The third experiments examined the effect of unequal probabilities. Our results support the view that monkeys can learn from non-conspecific actors through vicarious reward, even a symbolic task like the token-exchange task.     

Dispersal of sweet pignut hickory in a year of low fruit production,and the influence of predation by a curculionid beetle

Summary The rate at which fallen hickory nuts are removed from beneath the parent tree, and the effect on this rate of the seed predatorConotrachelus affinis, was studied in an oak-hickory forest in southeastern Michigan, USA, during a year in which few nuts were produced. The trees responded toConotrachelus, which destroyed half the nut crop, by aborting inviable nuts during the summer. The seed dispersers, mostly gray squirrels, removed fallen nuts rapidly, showing the ability to distinguish viable nuts and remove them preferentially. The number of nuts removed in a week varies directly with the number available, and removal rate increases when many viable nuts are falling. The death of most seeds before dispersal, and the squirrels' efficiency at foraging on nuts and recovering them after burial, imply that successful hickory reproduction takes place only in years of heavy nut production.