Insights into the evolutionary history of the most skilled tool-handling platyrrhini monkey: Sapajus libidinosus from the Serra da Capivara National Park.

Sapajus libidinosus members of the Pedra Furada group, living in the Serra da Capivara National Park, use stone tools in a wider variety of behaviors than any other living animal, except humans. To rescue the evolutionary history of the Caatinga S. libidinosus and identify factors that may have contributed to the emergence and maintenance of their tool-use culture, we conducted fieldwork seasons to obtain biological samples of these capuchin monkeys. UsingCYTBsequences, we show a discrete but constant population growth from the beginning of the Holocene to the present, overlapping the emergence of the Caatinga biome. Our habitat suitability reconstruction reports the presence of plants whose hard fruits, seeds, or roots are processed by capuchins using tools. TheS. libidinosusindividuals in the Caatinga were capable of dynamically developing and maintaining their autochthonous culture thanks to: a) cognitive capacity to generate and execute innovation under selective pressure; b) tolerance favoring learning and cultural inheritance; c) an unknown genetic repertoire that underpins the adaptive traits; d) a high degree of terrestriality; e) presence and abundance of natural resources, which makes some places "hot spots" for innovation, and cultural diversification within a relatively short time.

Wild monkeys flake stone tools.

Our understanding of the emergence of technology shapes how we view the origins of humanity. Sharp-edged stone flakes, struck from larger cores, are the primary evidence for the earliest stone technology. Here we show that wild bearded capuchin monkeys (Sapajus libidinosus) in Brazil deliberately break stones, unintentionally producing recurrent, conchoidally fractured, sharp-edged flakes and cores that have the characteristics and morphology of intentionally produced hominin tools. The production of archaeologically visible cores and flakes is therefore no longer unique to the human lineage, providing a comparative perspective on the emergence of lithic technology. This discovery adds an additional dimension to interpretations of the human Palaeolithic record, the possible function of early stone tools, and the cognitive requirements for the emergence of stone flaking.

Ontogeny and sex differences in object manipulation and probe tool use by wild tufted capuchin monkeys (Sapajus libidinosus).

Tufted capuchin monkeys (Sapajus spp.) are the only Neotropical Primates that regularly use tools in the wild, but only one population of bearded capuchin monkeys (Sapajus libidinosus) is known to habitually use sticks as probes. In this population, males are typically the only sex to use stick tools, something unexpected, since there are no obvious physical constraints, and females do use stone tools in the wild and sticks in experimental conditions. We investigated the development of probe tool use in eight infants to clarify whether social influences on learning varied between the sexes, as tool use learning by capuchin monkeys is a socially biased process. We found that in the first 10 months of age, females manipulate sticks as much as males, but after 10-12 months of age, males begin to manipulate them at higher frequencies. We examined if social connections-as opportunities for social learning-could explain this difference and verified that, on close distance social networks, infant males and females have similar connections with older males. However, males observe probe tool use events more often than females when close to such events. The higher frequency of manipulation of sticks, as well as the higher rates of probe tool use observation, appear to be the key to understand why only males are probe tool users in this population. Since there are only male potential models of probe use, a sex motivational bias could explain the sex difference in observation; a bias in observation could explain the differences in manipulation-and manipulation rates would certainly influence the chances of individual, trial-and-error learning (a case of "local/stimulus enhancement").

The effects of tradition on problem solving by two wild populations of bearded capuchin monkeys in a probing task.

The effects of culture on individual cognition have become a core issue among cultural primatologists. Field studies with wild populations provide evidence on the role of social cues in the ontogeny of tool use in non-human primates, and on the transmission of such behaviours over generations through socially biased learning. Recent experimental studies have shown that cultural knowledge may influence problem solving in wild populations of chimpanzees. Here, we present the results from a field experiment comparing the performance of bearded capuchin monkeys (Sapajus libidinosus) from two wild savannah populations with distinct toolkits in a probing task. Only the population that already exhibited the customary use of probing tools succeeded in solving the new problem, suggesting that their cultural repertoire shaped their approach to the new task. Moreover, only this population, which uses stone tools in a broader range of contexts, tried to use them to solve the problem. Social interactions can affect the formation of learning sets and they affect the performance of the monkeys in problem solving. We suggest that behavioural traditions affect the ways non-human primates solve novel foraging problems using tools.

Diversity of nutcracking tool sites used by Sapajus libidinosus in Brazilian Cerrado.

Cracking nuts with tools is a behavior documented in a small number of populations of tufted capuchins, mainly in semi-arid Caatinga and Caatinga-Cerrado transitional environments of northeastern Brazil. Only one of these populations inhabits the less arid Cerrado in Central Brazil, where environments are composed of a heterogeneous mosaic of fields, savannas and forest formations. We conducted surveys in 10 of 20 localities where nutcracking by capuchins was reported by the local inhabitants in the Cerrrado of Northern Goiás and Tocantins. Our purpose was to evaluate nutcracking sites (anvils and associated hammers and nuts) based on indirect evidence of extensive pounding of nuts and seeds. Nutcracking was confirmed at all 10 surveyed localities. A total of 270 sites were identified. Surveyed localities included areas that were ecologically similar to those where capuchins crack nuts in Caatinga, as well as less arid localities with more typical Cerrado habitat. Anvils and hammers were made of materials including quartz, limestone, sandstone and wood, and displayed a wider range of sizes (i.e., 60-3,750 g for hammers' weight) than reported at previously studied localities. Nuts of seven genera were found in association with anvils and hammers. We conclude that nutcracking by capuchins are not restricted to arid environments and argue that the occurrence and diversity of nutcracking tool sites result from complex interactions of environmental variables (e.g., availability of food and mineral resources, density of canopy cover) and social variables (e.g., spatial cohesiveness and tolerance among group members) that need to be examined through long-term research of habituated groups. Localities in the Cerrado of Northern Goiás and Tocantins vary considerable in the ecological conditions faced by wild groups, and therefore offer the opportunity to examine these interactions.

Toxic tasting: how capuchin monkeys avoid grasshoppers' chemical defenses.

Platyrrhines consume many species of arthropods in the order Orthoptera. Some species of orthopterans can produce chemical defenses that render them toxic or unpalatable and thus act as predator deterrents. These species include the stick grasshoppers (family Proscopiidae), which are widely distributed in the Caatinga biome in northeastern Brazil, which comprises part of the distribution of capuchin monkeys. Capuchin monkeys are omnivores and consume a wide variety of foods, including unpleasant-tasting, potentially toxic items, which they need to learn how to process. We describe the processing of stick grasshoppers (Stiphra sp.) by wild capuchin monkeys (Sapajus libidinosus) that live in Serra da Capivara National Park, Brazil, and compare how individuals of different age classes handle these potentially toxic food items. S. libidinosus predominantly avoided consuming the digestive tract, which contains toxic compounds, when feeding on stick grasshoppers. Immatures took longer than adults to process the stick grasshoppers, indicating that capuchins need to learn how to process the toxic digestive tract of these prey to avoid consuming it.

Greater tool use diversity is associated with increased terrestriality in wild capuchin monkeys.

Terrestriality was an essential factor in human evolution. Hominins' extensive use of the ground allowed exploring a new range of environments and their objects, including new resources and potential tool raw materials. Capuchin monkeys are primarily arboreal primates but are also the most prolific tool users among platyrrhines, customarily using stone tools on the ground due to physical limitations and material availability. OBJECTIVES: Our goals were to (1) measure the terrestriality levels of a group of capuchin monkeys and (2) test the hypothesis that terrestriality has a positive effect on the stone tool use variability because the increased time on the ground would offer more opportunities to interact with the available stones, leading to more innovations of tool use behaviors. We predict a more diversified use of stone tools in the population with a higher degree of terrestriality. MATERIALS AND METHODS: This study was on a group of capuchin monkeys (Sapajus libidinosus) at Serra da Capivara National Park (SCNP), Brazil. Scan sampling was done for 23 months, recording the behavior and substrate used by the individuals. RESULTS: The ground use rate was 41%, with no sex difference but an age difference: infants were less terrestrial than juveniles and adults. DISCUSSION: Compared to a population with a more limited tool use repertoire (Fazenda Boa Vista), SCNP adult capuchins are more terrestrial (43% v. 27%). Stone tool use diversity and terrestriality in capuchins appear to be positively correlated. Our results support this hypothesis and provide terrestriality measurements of the wild capuchin population with the most complex stone tool kit.

Wild robust capuchin monkey interactions with sympatric primates.

Examining interactions among sympatric primate species can provide interesting information about competition, cooperation, and avoidance between those species. Those interactions can be neutral, positive, or negative for the species involved. Capuchin monkeys are medium-sized primates that can encounter both larger and smaller primates in their varied habitats. Gracile capuchins (Cebus) are reported to present different types of interactions with other primates. Interactions with howler monkeys frequently include physical aggression, while interactions with spider monkeys are mostly threats and chases. Moreover, interaction types are not consistent across populations. Among robust capuchins (Sapajus spp.), however, no reports have been published. Here we describe and classify encounters of Sapajus libidinosus and S. nigritus with Alouatta caraya, A. guariba, Brachyteles arachnoides, and Callithrix jacchus in three sites in the environments of Cerrado, Caatinga (savannah-like), and Atlantic forest, and compare the interaction patterns among sites and different group sizes. The latter is a factor that can influence the outcome, and we expected capuchins in larger groups to be more aggressive toward other primates. Our results of 8421 h of total contact with the capuchin groups show that, indeed, capuchins in sites with larger groups presented aggressive interactions with higher frequency. However, the other species' body size also seems important as smaller primates apparently avoided capuchins, and interactions with the larger muriquis were mostly neutral for the capuchin. Capuchins showed neutral or aggressive behaviors toward howler monkeys, with differences between the rainforest and savannah groups. We found that robust capuchins can present aggressive interactions even to primates larger than themselves and that aggressive behavior was the most common response in populations living in larger groups and drier environments.

Means to an end: neotropical parrots manage to pull strings to meet their goals.

Although parrots share with corvids and primates many of the traits believed to be associated with advanced cognitive processing, knowledge of parrot cognition is still limited to a few species, none of which are Neotropical. Here we examine the ability of three Neotropical parrot species (Blue-Fronted Amazons, Hyacinth and Lear's macaws) to spontaneously solve a novel physical problem: the string-pulling test. The ability to pull up a string to obtain out-of-reach food has been often considered a cognitively complex task, as it requires the use of a sequence of actions never previously assembled, along with the ability to continuously monitor string, food and certain body movements. We presented subjects with pulling tasks where we varied the spatial relationship between the strings, the presence of a reward and the physical contact between the string and reward to determine whether (1) string-pulling is goal-oriented in these parrots, (2) whether the string is recognized as a means to obtain the reward and (3) whether subjects can visually determine the continuity between the string and the reward, selecting only those strings for which no physical gaps between string and reward were present. Our results show that some individuals of all species were able to use the string as a means to reach a specific goal, in this case, the retrieval of the food treat. Also, subjects from both macaw species were able to visually determine the presence of physical continuity between the string and reward, making their choices consistently with the recognition that no gaps should be present between the string and the reward. Our findings highlight the potential of this taxonomic group for the understanding of the underpinnings of cognition in evolutionarily distant groups such as birds and primates.

Fallback foraging as a way of life: using dietary toughness to compare the fallback signal among capuchins and implications for interpreting morphological variation.

The genus Cebus is one of the best extant models for examining the role of fallback foods in primate evolution. Cebus includes the tufted capuchins, which exhibit skeletal features for the exploitation of hard and tough foods. Paradoxically, these seemingly "specialized" taxa belong to the most ubiquitous group of closely related primates in South America, thriving in a range of different habitats. This appears to be a consequence of their ability to exploit obdurate fallback foods. Here we compare the toughness of foods exploited by two tufted capuchin species at two ecologically distinct sites; C. apella in a tropical rainforest, and C. libidinosus in a cerrado forest. We include dietary data for one untufted species (C. olivaceus) to assess the degree of difference between the tufted species. These data, along with information on skeletal morphology, are used to address whether or not a fallback foraging species exhibits a given suite of morphological and behavioral attributes, regardless of habitat. Both tufted species ingest and masticate a number of exceedingly tough plant tissues that appear to be used as fallback resources, however, C. libidinosus has the toughest diet both in terms of median and maximal values. Morphologically, C. libidinosus is intermediate in absolute symphyseal and mandibular measurements, and in measures of postcranial robusticity, but exhibits a higher intermembral index than C. apella. We propose that this incongruence between dietary toughness and skeletal morphology is the consequence of C. libidinosus' use of tools while on the ground for the exploitation of fallback foods.

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.

Three thousand years of wild capuchin stone tool use.

The human archaeological record changes over time. Finding such change in other animals requires similar evidence, namely, a long-term sequence of material culture. Here, we apply archaeological excavation, dating and analytical techniques to a wild capuchin monkey (Sapajus libidinosus) site in Serra da Capivara National Park, Brazil. We identify monkey stone tools between 2,400 and 3,000 years old and, on the basis of metric and damage patterns, demonstrate that capuchin food processing changed between ~2,400 and 300 years ago, and between ~100 years ago and the present day. We present the first example of long-term tool-use variation outside of the human lineage, and discuss possible mechanisms of extended behavioural change.

Learning generalization in problem solving by a blue-fronted parrot (Amazona aestiva).

Pepperberg (The Alex studies: cognitive and communicative abilities of gray parrots. Harvard University Press, Cambridge;1999) showed that some of the complex cognitive capabilities found in primates are also present in psittacine birds. Through the replication of an experiment performed with cotton-top tamarins (Saguinus oedipus oedipus) by Hauser et al. (Anim Behav 57:565-582; 1999), we examined a blue-fronted parrot's (Amazona aestiva) ability to generalize the solution of a particular problem in new but similar cases. Our results show that, at least when it comes to solving this particular problem, our parrot subject exhibited learning generalization capabilities resembling the tamarins'.

Ontogeny of manipulative behavior and nut-cracking in young tufted capuchin monkeys (Cebus apella): a perception-action perspective.

How do capuchin monkeys learn to use stones to crack open nuts? Perception-action theory posits that individuals explore producing varying spatial and force relations among objects and surfaces, thereby learning about affordances of such relations and how to produce them. Such learning supports the discovery of tool use. We present longitudinal developmental data from semifree-ranging tufted capuchin monkeys (Cebus apella) to evaluate predictions arising from Perception-action theory linking manipulative development and the onset of tool-using. Percussive actions bringing an object into contact with a surface appeared within the first year of life. Most infants readily struck nuts and other objects against stones or other surfaces from 6 months of age, but percussive actions alone were not sufficient to produce nut-cracking sequences. Placing the nut on the anvil surface and then releasing it, so that it could be struck with a stone, was the last element necessary for nut-cracking to appear in capuchins. Young chimpanzees may face a different challenge in learning to crack nuts: they readily place objects on surfaces and release them, but rarely vigorously strike objects against surfaces or other objects. Thus the challenges facing the two species in developing the same behavior (nut-cracking using a stone hammer and an anvil) may be quite different. Capuchins must inhibit a strong bias to hold nuts so that they can release them; chimpanzees must generate a percussive action rather than a gentle placing action. Generating the right actions may be as challenging as achieving the right sequence of actions in both species. Our analysis suggests a new direction for studies of social influence on young primates learning sequences of actions involving manipulation of objects in relation to surfaces.

Cognition in an ever-changing world: climatic variability is associated with brain size in Neotropical parrots.

Research on the conditions favoring the evolution of complex cognition and its underlying neural structures has increasingly stressed the role of environmental variability. These studies suggest that the ability to learn, behave flexibly and innovate would be favored under unpredictable variations in the availability of resources, as it would enable organisms to adjust to novel conditions. Despite the growing number of studies based on the idea that larger-brained organisms would be better prepared to cope with environmental challenges, direct testing of the association between brain size and environmental variability per se remains scant. Here we focus on Neotropical parrots as our model group and test the hypothesis that if relatively larger brains were favored in climatically variable environments, larger-brained species should currently tolerate a higher degree of environmental uncertainty. Although we show that there are also other factors underlying the dynamics of brain size variation in this group, our results support the hypothesis that proportionally larger-brained species are more tolerant to climatic variability, both on a temporal and spatial scale. Additionally, they suggest that the differences in relative brain size among Neotropical parrots represent multiple, recent events in the evolutionary history of the group, and are particularly tied to an increased dependence on more open and climatically unstable habitats. As this is the first study to present evidence of the link between brain size and climatic variability in birds, our findings provide a step towards understanding the potential benefits underlying variation in brain size and the maintenance of highly enlarged brains in this and other groups.

Food or threat? Wild capuchin monkeys (Sapajus libidinosus) as both predators and prey of snakes.

Snakes present a hazard to primates, both as active predators and by defensive envenomation. This risk might have been a selective pressure on the evolution of primate visual and cognitive systems, leading to several behavioral traits present in human and non-human primates, such as the ability to quickly learn to fear snakes. Primates seldom prey on snakes, and humans are one of the few primate species that do. We report here another case, the wild capuchin monkey (Sapajus libidinosus), which preys on snakes. We hypothesized that capuchin monkeys, due to their behavioral plasticity, and cognitive and visual skills, would be capable of discriminating dangerous and non-dangerous snakes and behave accordingly. We recorded the behavioral patterns exhibited toward snakes in two populations of S. libidinosus living 320 km apart in Piauí, Brazil. As expected, capuchins have a fear reaction to dangerous snakes (usually venomous or constricting snakes), presenting mobbing behavior toward them. In contrast, they hunt and consume non-dangerous snakes without presenting the fear response. Our findings support the tested hypothesis that S. libidinosus are capable of differentiating snakes by level of danger: on the one hand they protect themselves from dangerous snakes, on the other hand they take opportunities to prey on non-dangerous snakes. Since capuchins and humans are both predators and prey of snakes, further studies of this complex relationship may shed light on the evolution of these traits in the human lineage.

Stone tool use by wild capuchin monkeys (Sapajus libidinosus) at Serra das Confusões National Park, Brazil.

Capuchin monkeys (Sapajus spp.) are proficient tool users, and the use of stone tools occurs in several populations, mostly to crack open encased foods. Two well-studied Brazilian populations of Sapajus libidinosus inhabit Fazenda Boa Vista and Serra da Capivara National Park and present different behavioral sets regarding tool use. Serra das Confusões National Park (SCoNP) lies between those sites, but little is known about the capuchin monkey population that lives there. To begin unraveling the capuchin behavior in this area, we conducted a brief survey for tool use sites. We found indirect evidence that capuchin monkeys at SCoNP use stone hammers to crack open at least four species of seeds and fruits. Plant reproductive parts there are processed with stone tools in a similar pattern to the other sites. Further study is needed to directly observe tool use by capuchin monkeys at SCoNP, verify the occurrence of other possible types of tool use in this population, and thus fully compare their tool use repertoire to that of other populations.

Repellent efficacy of formic acid and the abdominal secretion of carpenter ants (Hymenoptera: Formicidae) against Amblyomma ticks (Acari: Ixodidae).

Formic acid is a substance produced by some ants for defense, trail marking, and recruitment. Some animals are known to rub ants or other arthropods on parts of their plumage or fur to anoint themselves with released substances. A recent study with a semifree-ranging group of capuchin monkeys, Cebus apella L., in the Tietê Ecological Park, Sao Paulo, Brazil, an area of occurrence of the tick species Amblyomma cajennense (F.), revealed that "anting" with carpenter ants, Camponotus rufipes F. (Hymenoptera: Formicidae), occurs frequently, especially during the A. cajennense subadult season. Based on these observations, we tested the repellent effect of the formic acid and the ants themselves against A. cajennense and Amblyomma incisum Neumann nymphs, and Amblyomma parcum Aragdo adult ticks in the laboratory. The results revealed a significant repellent effect of formic acid and ant secretion, and a significant duration of the repellent effect. The results suggest that the anting behavior of capuchin monkeys, and other vertebrates, may be related with repellence of ticks and other ectoparasites.

Digging up food: excavation stone tool use by wild capuchin monkeys.

Capuchin monkeys at Serra da Capivara National Park (SCNP) usually forage on the ground for roots and fossorial arthropods, digging primarily with their hands but also using stone tools to loosen the soil and aid the digging process. Here we describe the stone tools used for digging by two groups of capuchins on SCNP. Both groups used tools while digging three main food resources: Thiloa glaucocarpa tubers, Ocotea sp roots, and trapdoor spiders. One explanation for the occurrence of tool use in primates is the "necessity hypothesis", which states that the main function of tool use is to obtain fallback food. We tested for this, but only found a positive correlation between plant food availability and the frequency of stone tools' use. Thus, our data do not support the fallback food hypothesis for the use of tools to access burrowed resources.

Primate archaeology evolves.

Since its inception, archaeology has traditionally focused exclusively on humans and our direct ancestors. However, recent years have seen archaeological techniques applied to material evidence left behind by non-human animals. Here, we review advances made by the most prominent field investigating past non-human tool use: primate archaeology. This field combines survey of wild primate activity areas with ethological observations, excavations and analyses that allow the reconstruction of past primate behaviour. Because the order Primates includes humans, new insights into the behavioural evolution of apes and monkeys also can be used to better interrogate the record of early tool use in our own, hominin, lineage. This work has recently doubled the set of primate lineages with an excavated archaeological record, adding Old World macaques and New World capuchin monkeys to chimpanzees and humans, and it has shown that tool selection and transport, and discrete site formation, are universal among wild stone-tool-using primates. It has also revealed that wild capuchins regularly break stone tools in a way that can make them difficult to distinguish from simple early hominin tools. Ultimately, this research opens up opportunities for the development of a broader animal archaeology, marking the end of archaeology's anthropocentric era.