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.

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.

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.

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 effect of verbal information about model's competence on overimitation by preschool children.

Overimitation is defined by a tendency to copy all actions executed by a model, even the clearly irrelevant ones. The motivational mechanisms and functionality of overimitation are still not well understood, but its possible adaptive meaning could be related to causal opacity of a great part of socially learned behaviors. This phenomenon has been widely replicated in several contexts and has been observed in the behavior of children over 2 years of age and even in adults. Despite the seeming robustness of overimitation, studies have shown that it is sensitive to some characteristics of a model observed such as age, familiarity, proficiency, and reputation. Our work intended to investigate the effect of information about the competence of an adult model on the copying of irrelevant actions by preschool children (5 years old) in a task. We tested the influence of self-declared information about the model competence and of the same kind of information given by third parties in a conversation about the model. Our results reveal no effect of both "self-declared competence" and "reputation" biases on overimitation. We discuss that this result may have occurred because other information available to participants, and not manipulated by us, was used to infer model competence such as the model's age and success in the task directly observed by the participants. Another potential explanation is that children use a "copy all, correct later" strategy in a context where only one model is available.

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.

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.

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.

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.

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.

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.

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.

Pre-Columbian monkey tools.

Stone tools reveal worldwide innovations in human behaviour over the past three million years [1]. However, the only archaeological report of pre-modern non-human animal tool use comes from three Western chimpanzee (Pan troglodytes verus) sites in Côte d'Ivoire, aged between 4.3 and 1.3 thousand years ago (kya) [2]. This anthropocentrism limits our comparative insight into the emergence and development of technology, weakening our evolutionary models [3]. Here, we apply archaeological techniques to a distinctive stone tool assemblage created by a non-human animal in the New World, the Brazilian bearded capuchin monkey (Sapajus libidinosus). Wild capuchins at Serra da Capivara National Park (SCNP) use stones to pound open defended food, including locally indigenous cashew nuts [4], and we demonstrate that this activity dates back at least 600 to 700 years. Capuchin stone hammers and anvils are therefore the oldest non-human tools known outside of Africa, opening up to scientific scrutiny questions on the origins and spread of tool use in New World monkeys, and the mechanisms - social, ecological and cognitive - that support primate technological evolution.

Vertical bipedal locomotion in wild bearded capuchin monkeys (Sapajus libidinosus).

When carrying objects, nonhuman primates often show bipedal locomotion. Studies of primate bipedality, however, in both nature and captivity, have concentrated on locomotion on horizontal substrates, either terrestrially or arboreally. No observational or experimental study seems to have looked at non-horizontal bipedality, yet we show here that it occurs often in nature in Sapajus libidinosus, the bearded capuchin monkey. The context is transport of small food items from source to site of consumption, in which the monkeys usually carry handfuls of maize kernels over several meters' distance, both on the ground and in the trees. Most impressively, over a fifth of such bouts are done vertically, when the tree trunk is fully upright. Such vertical bipedality, with or without transport, apparently has not been reported before.

Sequential organization and optimization of the nut-cracking behavior of semi-free tufted capuchin monkeys (Sapajus sp.).

Stone-aided nut-cracking requires the coordination of three elements: the agent must assemble nuts, a "hammer" stone and an "anvil." Under naturalistic settings, nut-cracking sites, constituted of anvil-like surfaces and already containing a hammer stone, can be fairly stable, lasting as long as the "hammer" stays in place. In an experiment with a semi-free-ranging group of tufted capuchin monkeys (Sapajus sp.) we observed the behavioral sequences leading to nut-cracking. We positioned nuts, hammer, and anvil at the vertices of a 10-m-sided equilateral triangle. Thus, to crack a nut the individuals had to visit the vertices and gather the movable elements (nut and hammer) at the anvil. Under such conditions, the monkeys systematically employed a nut-hammer-anvil vertex visit sequence, one of the shortest and more cost-effective possible routes. In the following experiment, we examined whether the gathering of the hammer after the nuts resulted solely from a "nut first" strategy or if the monkeys were also minimizing hammer transport costs. We positioned two hammers, of the same weight, at different distances from the nuts and anvil, so the cost of hammer transportation (energy and risk of injury) would be higher or lower depending on the choice of hammer (the hammer closer to the nuts being farther from the anvil). We found that, instead of collecting the closest hammer, after collecting the nut, the monkeys systematically chose the hammer closer to (and beyond) the anvil, thus minimizing transport costs.

A análise do comportamento no contexto do estudo evolucionista do comportamento social e da cultura / Behavior analysis in the context of the evolutionary study of social behavior and culture / El análisis de la conducta en el contexto del estudio evolucionista de la conducta social y cultura

A Análise do Comportamento pode ser entendida como uma perspectiva voltada para o estudo evolucionista do comportamento social e da cultura. A caracterização do comportamento social nessa área e pesquisas recentes sobre metacontingências e macrocontingências são contribuições nesse sentido. Outras perspectivas evolucionistas mais próximas da Biologia também têm produzido diversas teorias e resultados sobre o tema, mas sem dialogar com a Análise do Comportamento, que, por sua vez, pouco debate as contribuições dessas outras perspectivas. Este trabalho destaca possíveis convergências e complementaridades entre a Análise do Comportamento e estudos sobre aprendizagem social em animais não-humanos, construção de nicho e evolução cultural, visando estimular o diálogo entre pesquisadores de diferentes perspectivas evolucionistas que estudam comportamento social e cultura.

Behavior Analysis may be regarded as a perspective that tackles the evolutionary study of social behavior and culture. Social behavior's characterization in this field and recent researches on metacontingencies and macrocontingencies are contributions in this direction. Other evolutionary perspectives, closest to Biology, have also produced theories and evidences on this theme, but without dialogue with Behavior Analysis, which, by its turn, discusses little this other perspectives' contributions. This paper highlights possible convergences and complementarities between Behavior Analysis and studies on social learning in nonhuman animals, niche construction, and cultural evolution, aiming to enhance dialogues among researchers from different evolutionary perspectives studying social behavior and culture.

El Análisis de la Conducta puede ser vista desde una perspectiva enfocada al estudio evolucionista de la conducta social y cultura. La caracterización de la conducta social en esa área y estudios recientes sobre metacontingencias y macrocontingencias son algunas de sus contribuciones. Otras perspectivas evolucionistas aproximadas a la Biología también han producido diversas teorías y resultados sobre el tema, pero sin interactuar con el Análisis de la Conducta, que al mismo tiempo, poco debata las contribuciones de esas otras perspectivas. Este trabajo destaca posibles convergencias e complementaciones entre el Análisis de la Conducta y los estudios sobre aprendizaje social en animales no humanos, construcción de nicho y evolución cultural, con el objetivo de estimular el dialogo entre investigadores de diferentes perspectivas evolucionistas que estudian la conducta social y la cultura.

A Análise do Comportamento no contexto do estudo evolucionista do comportamento social e da cultura / Behavior Analysis in the context of the evolutionary study of social behavior and culture / El Análisis de la Conducta en el contexto del estudio evolucionista de la conducta social y cultura

ResumoA Análise do Comportamento pode ser entendida como uma perspectiva voltada para o estudo evolucionista do comportamento social e da cultura. A caracterização do comportamento social nessa área e pesquisas recentes sobre metacontingências e macrocontingências são contribuições nesse sentido. Outras perspectivas evolucionistas mais próximas da Biologia também têm produzido diversas teorias e resultados sobre o tema, mas sem dialogar com a Análise do Comportamento, que, por sua vez, pouco debate as contribuições dessas outras perspectivas. Este trabalho destaca possíveis convergências e complementaridades entre a Análise do Comportamento e estudos sobre aprendizagem social em animais não-humanos, construção de nicho e evolução cultural, visando estimular o diálogo entre pesquisadores de diferentes perspectivas evolucionistas que estudam comportamento social e cultura.(AU)

AbstractBehavior Analysis may be regarded as a perspective that tackles the evolutionary study of social behavior and culture. Social behavior's characterization in this field and recent researches on metacontingencies and macrocontingencies are contributions in this direction. Other evolutionary perspectives, closest to Biology, have also produced theories and evidences on this theme, but without dialogue with Behavior Analysis, which, by its turn, discusses little this other perspectives' contributions. This paper highlights possible convergences and complementarities between Behavior Analysis and studies on social learning in nonhuman animals, niche construction, and cultural evolution, aiming to enhance dialogues among researchers from different evolutionary perspectives studying social behavior and culture.(AU)

ResumenEl Análisis de la Conducta puede ser vista desde una perspectiva enfocada al estudio evolucionista de la conducta social y cultura. La caracterización de la conducta social en esa área y estudios recientes sobre metacontingencias y macrocontingencias son algunas de sus contribuciones. Otras perspectivas evolucionistas aproximadas a la Biología también han producido diversas teorías y resultados sobre el tema, pero sin interactuar con el Análisis de la Conducta, que al mismo tiempo, poco debata las contribuciones de esas otras perspectivas. Este trabajo destaca posibles convergencias e complementaciones entre el Análisis de la Conducta y los estudios sobre aprendizaje social en animales no humanos, construcción de nicho y evolución cultural, con el objetivo de estimular el dialogo entre investigadores de diferentes perspectivas evolucionistas que estudian la conducta social y la cultura.(AU)

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.

Sexual bias in probe tool manufacture and use by wild bearded capuchin monkeys.

Here we examine data from a two-year research on the use of sticks as probes by two groups of wild capuchin monkeys (Sapajus libidinosus) in Serra da Capivara National Park (PI), Brazil. The use of sticks as probes is not usually observed among wild tufted capuchin (Sapajus spp.) populations, having been reported as a customary behavior only in SCNP groups. Probe tools are used to access small prey (insects or lizards) in rock cracks or tree trunks, or honey from wasps' nests, and also to poke toads and poisonous snakes. Probe use is, so far, the only known case in which wild capuchins modify objects used as tools: branches are trimmed off, and tips, thinned. Tool preparation episodes involved up to four modification steps. Contrary to the stone tools used to crack hard nuts, probe tools don't present any weight constraint for use by females, but there is nevertheless a strong male bias (97%) in the occurrence of probe tool use. There are also no diet biases that could explain this difference. Although males hunt more often than females, the latter main prey items are lizards, which are also the main targets of probe tool use. One possibility is that females may have fewer social opportunities to learn about probe tools.