Mapping nut-cracking in a new population of wild capuchin monkeys (Sapajus libidinosus) at Ubajara National Park, Brazil.

Populations of bearded capuchin monkeys (Sapajus libidinosus) vary in their tool use behaviors, with some of this divergence regarded as culturally determined. The use of stone tools, primarily to crack open encased foods, is widespread among bearded capuchins living in dry habitats (Caatinga and Cerrado). Significant diversity in targets, processed foods, material, and size of tools is observed across populations. However, so far, only a few sites have been systematically studied, and we are still distant from a representative picture of the range of variation in capuchins' culture. In this study, we did a systematic assessment of stone tool use sites in the Ubajara National Park (UNP), in the Caatinga region of Ceará, Brazil, recording and measuring stone tools, processed foods, and available lithic resources as part of an extensive comparative research, the CapCult project. We found indirect and direct evidence that capuchin monkeys at UNP customarily use hammerstones and anvils to process at least two species of palm nuts, macauba (Acrocomia aculeata) and the harder babaçu (Attalea speciosa). Most of the anvils were rock surfaces and had leftovers of only one palm nut species. The hammerstones used to process both palm nuts were not significantly different in weight, although the ones used for Ac. aculeata were longer. We found a higher frequency of nut-cracking sites in the drier lowland area of the park, reflecting differences in the density of the most common palm species, Ac. aculeata, and availability of raw stone material. The stone tool use observed in UNP is within the scope of previously reported in savannah capuchin populations. Our study widens the knowledge of stone tool-use diversity in wild capuchin monkeys, which could contribute to shaping conservation policy, including cultural traits.

Exploring the diversity of AVPR2 in Primates and its evolutionary implications.

The current study focuses on the investigation of AVPR2 (VTR2C) protein-coupled receptor variants specific to different primate taxa. AVPR2 is activated by the neurohormone AVP, which modulates physiological processes, including water homeostasis. Our findings reveal positive selection at three AVPR2 sites at positions 190, 250, and 346. Variation at position 250 is associated with human Congenital Nephrogenic Diabetes Insipidus (cNDI), a condition characterized by excessive water loss. Other 13 functional sites with potential adaptive relevance include positions 185, 202, 204, and 252 associated with cNDI. We identified SH3-binding motifs in AVPR2's ICL3 and N-terminus domains, with some losses observed in clades of Cercopithecidae, Callitrichinae, and Atelidae. SH3-binding motifs are crucial in regulating cellular physiology, indicating that the differences may be adaptive. Co-evolution was found between AVPR2 residues and those in the AVP signal peptide/Neurophysin-2 and AQP2, other molecules in the same signaling cascade. No significant correlation was found between these Primates' taxon-specific variants and the bioclimatic variables of the areas where they live. Distinct co-evolving amino acid sequences in functional sites were found in Platyrrhini and Catarrhini, which may have adaptive implications involving glucocorticoid hormones, suggesting varied selective pressures. Further studies are required to confirm these results.

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.

A primate model for the origin of flake technology.

When and how human ancestors first used tools remains unknown, despite intense research into the origins of technology. It has been hypothesized that the evolutionary roots of stone flake technology has its origin in percussive behavior. Before intentional stone flaking, hominins potentially engaged in various percussive behaviors resulting in accidental flake detachments. We refer to this scenario as the 'by-product hypothesis.' In this scenario, repeated detachments of sharp stone fragments eventually resulted in intentional flake production. Here, we tested the circumstances of accidental flake production as a by-product of percussive foraging in wild capuchin monkeys (Sapajus libidinosus) from Brazil, the only nonhuman primate known to habitually produce sharp-edged flakes through a percussive behavior. We conducted field experiments where we tested the potential for accidental flake production during nut cracking. We provided three different types of stone with varied material properties as anvils to assess the circumstances in which accidental production of sharp-edged flakes occurs during nut cracking. A further freehand knapping experiment, with the raw material that exhibited accidental flake detachments, allows a direct comparison of flakes that have been intentionally produced by an experienced knapper and flakes produced during nut cracking by capuchin monkeys. Our results show that raw material quality and morphology significantly affect the rate of sharp-edged flake production as well as the resulting lithic signature of this behavior. In addition, accidental flakes produced during capuchin nut cracking on highly isotropic raw material are similar in many respects to intentionally produced flakes by a human knapper. Our field experiments highlight the fact that nut-cracking behavior can lead to the unintentional production of substantial quantities of sharp-edged flakes and therefore supports the 'by-product hypothesis' as a potential mechanism for the emergence of hominin flake technology.

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").

Analysis of sea almond (Terminalia catappa) cracking sites used by wild Burmese long-tailed macaques (Macaca fascicularis aurea).

Nut-cracking is shared by all non-human primate taxa that are known to habitually use percussive stone tools in the wild: robust capuchins (Sapajus spp.), western chimpanzees (Pan troglodytes verus), and Burmese long-tailed macaques (Macaca fascicularis aurea). Despite opportunistically processing nuts, Burmese long-tailed macaques predominantly use stone tools to process mollusks in coastal environments. Here, we present the first comprehensive survey of sea almond (Terminalia catappa) nut-cracking sites created by macaques. We mapped T. catappa trees and nut-cracking sites that we encountered along the intertidal zone and forest border on the coasts of Piak Nam Yai Island, Thailand. For each nut-cracking site, we measured the physical properties (i.e., size, weight, use-wear) of hammer stones and anvils. We found that T. catappa trees and nut-cracking sites primarily occurred on the western coast facing the open sea, and cracking sites clusters around the trees. We confirmed previous results that nut cracking tools are among the heaviest tools used by long-tailed macaques; however, we found our sample of T. catappa stone tools lighter than a previously collected sea almond sample that, unlike our sample, was collected immediately after use within the intertidal zone. The difference was likely the result of tidal influences on tool-use sites. We also found that tool accumulations above the intertidal region do not resemble those within them, possibly leading to incomplete assessments of macaque stone tools through archaeological techniques that would use these durable sites.

Cashew Nut Positioning during Stone Tool Use by Wild Bearded Capuchin Monkeys (Sapajus libidinosus).

Wild capuchin monkeys (Sapajus libidinosus) at Serra da Capivara National Park, Brazil, regularly use stone tools to break open cashew nuts (Anacardium spp.). Here we examine 2 approaches used by the capuchins to position the kidney-shaped cashew nuts on an anvil before striking with a stone tool. Lateral positioning involves placing the nut on its flatter, more stable side, therefore requiring less attention from the monkey during placement. However, the less stable and never previously described arched position, in which the nut is balanced with its curved side uppermost, requires less force to crack the outer shell. We observed cashew nut cracking in a field experimental setting. Only 6 of 20 adults, of both sexes, were observed to deliberately place cashew nuts in an arched position, which may indicate that the technique requires time and experience to learn. We also found that use of the arched position with dry nuts, but not fresh, required, in 63% of the time, an initial processing to remove one of the cashew nut lobes, creating a more stable base for the arch. This relatively rare behaviour appears to have a complex ontogeny, but further studies are required to establish the extent to which social learning is involved.

Wild capuchin monkeys use stones and sticks to access underground food.

Primates employ different tools and techniques to overcome the challenges of obtaining underground food resources. Humans and chimpanzees are known to tackle this problem with stick tools and one population of capuchin monkeys habitually uses stone tools. Although early hominids could have used stones as digging tools, we know little about when and how these could be useful. Here, we report a second primate population observed using stone tools and the first capuchin monkey population to habitually use the 'stick-probing' technique for obtaining underground resources. The bearded capuchin monkeys (Sapajus libidinosus) from Ubajara National Park, Brazil, use 'hands-only' and 'stone-digging' techniques for extracting underground storage organs and trapdoor spiders. Males also use 'stick-probing' and 'stone-stick' techniques for capturing trapdoor spiders. Tool use does not increase success in obtaining these resources. Stone-digging is less frequent in this population than in the only other known population that uses this technique. Females use stones in a lower proportion of their digging episodes than males in both populations. Ecological and cultural factors potentially influence technique choice and sex differences within and between populations. This population has a different pattern of underground food exploration using tools. Comparing this population with others and exploring the ecological and cultural factors under which capuchin monkeys employ different tools and techniques will allow us to better understand the pressures that may have shaped the evolution of those behaviors in primates.

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.

From molecular variations to behavioral adaptations: Unveiling adaptive epistasis in primate oxytocin system.

OBJECTIVE: Our primary objective was to investigate the variability of oxytocin (OT) and the GAMEN binding motif within the LNPEP oxytocinase in primates. MATERIALS AND METHODS: We sequenced the LNPEP segment encompassing the GAMEN motif in 34 Platyrrhini species, with 21 of them also sequenced for the OT gene. Our dataset was supplemented with primate sequences of LNPEP, OT, and the oxytocin receptor (OTR) sourced from public databases. Evolutionary analysis and coevolution predictions were made followed by the macroevolution analysis of relevant amino acids associated with phenotypic traits, such as mating systems, parental care, and litter size. To account for phylogenetic structure, we utilized two distinct statistical tests. Additionally, we calculated binding energies focusing on the interaction between Callithtrix jacchus VAMEN and Pro8OT. RESULTS: We identified two novel motifs (AAMEN and VAMEN), challenging the current knowledge of motif conservation in placental mammals. Coevolution analysis demonstrated a correlation between GAMEN, AAMEN, and VAMEN and their corresponding OTs and OTRs. Callithrix jacchus exhibited a higher binding energy between VAMEN and Pro8OT than orthologous molecules found in humans (GAMEN and Leu8OT). DISCUSSION: The coevolution of AAMEN and VAMEN with their corresponding OTs and OTRs suggests a functional relationship that could have contributed to specific reproductive and adaptive behaviors, including paternal care, social monogamy, and twin births, prominent traits in Cebidae species, such as marmosets and tamarins. Our findings underscore the coevolution of taxon-specific amino acids among the three studied molecules, shedding light on the oxytocinergic system as an adaptive epistatic repertoire in primates.

Life and death of a disabled wild capuchin monkey infant.

The evolutionary roots of care for injured, ill, and disabled group members remain unclear. The same can be said about care for dying and dead group members. Accumulating case reports in a variety of nonhuman primates can shed light on these origins. Here we provide a detailed account of interactions of a wild capuchin monkey mother and other group members with a disabled infant before and after its death. Limb disability caused the infant to be in unstable positions when carried, which appeared to increase the frequency of body readjustments by the adults and may have contributed to its death. After death, no adults other than the mother made contact with the corpse, but four immatures approached and touched it. The mother foraged only on flies surrounding the corpse while carrying it, stopped several times to set the corpse down on the branches, and let it finally fall as she leapt between trees. The difficulty of carrying disabled and dead individuals up in the trees may help to explain the scarcity of reports in platyrrhines, and suggests that terrestriality and increasing ease of bipedality may have contributed to the evolution of these behaviors in primates.

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.

Anointing variation across wild capuchin populations: a review of material preferences, bout frequency and anointing sociality in Cebus and Sapajus.

The frequency of anointing bouts and the materials used for self- and social anointing vary across capuchin species in captivity, but there is little published data on capuchin anointing in the wild. Here we present previously unpublished data on anointing behaviors from capuchin monkey populations at ten different field sites and incorporate these data into a review of the anointing literature for captive and wild capuchins. Using a comparative phylogenetic framework, we test four hypotheses derived primarily from captive literature for variation in anointing between wild untufted capuchins (Cebus) and tufted capuchins (Sapajus), including that (1) the frequency of anointing is higher in Cebus, (2) Cebus uses a higher proportion of plant species to insect species for anointing compared with Sapajus, (3) anointing material diversity is higher in Cebus, and (4) social indices of anointing are higher in Cebus. We found that wild Cebus anoints more with plant parts, including fruits, whereas wild Sapajus anoints more with ants and other arthropods. Cebus capucinus in particular uses more plant species per site for anointing compared with other capuchins and may specialize in anointing as an activity independent from foraging, whereas most other capuchin species tend to eat the substances they use for anointing. In agreement with captive studies, we found evidence that wild Cebus anoints at a significantly higher frequency than Sapajus. However, contrary to the captive literature, we found no difference in the range of sociality for anointing between Cebus and Sapajus in the wild. We review anointing in the context of other Neotropical primate rubbing behaviors and consider the evidence for anointing as self-medication; as a mechanism for enhanced sociality; and as a behavioral response to chemical stimuli.

Stone tools differences across three capuchin monkey populations: food's physical properties, ecology, and culture.

Robust capuchin monkeys (Sapajus) are known for processing mechanically challenging foods, having morphological adaptations to do so. However, several populations go beyond body limitations by using stone tools to expand their food range. Those populations use stones in a variety of ways, goals, and with different frequencies. Stone tool size correlates with the food's resistance within some populations. However, we have no detailed comparisons to identify if this correlation is the same across populations. This study described and compared stone raw material availability, food's physical properties (hardness and elasticity), and stone tool weight in three populations of bearded capuchin monkeys (Sapajus libidinosus), including a newly described site (Chapada dos Veadeiros National Park, CVNP). The differences we observed regarding stone tool weight selection among sites were not correlated to the food's physical properties we analyzed. Lithic resource availability could partly explain some differences in the stone tools used. However, the tool weight differences are larger than the raw material variance across sites, meaning some distinctions are possible behavioral traditions, such as the same fruit (Hymenaea) being processed with bigger than needed tools in CVNP than in the other two sites. Capuchin monkey behavioral variability in stone tool use can be caused by several interacting factors, from ecological to cultural.

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.

Evolutionary analysis of the anti-viral STAT2 gene of primates and rodents: Signature of different stages of an arms race.

STAT2 plays a strategic role in defending viral infection through the signaling cascade involving the immune system initiated after type I interferon release. Many flaviviruses target the inactivation or degradation of STAT2 as a strategy to impair this host's line of defense. Primates are natural reservoirs for a range of disease-causing flaviviruses (e.g., Zika, Dengue, and Yellow Fever virus), while rodents appear less susceptible. We analyzed the STAT2 coding sequence of 28 Rodentia species and 49 Primates species. Original data from 19 Platyrrhini species were sequenced for the SH2 domain of STAT2 and included in the analysis. STAT2 has many sites whose variation can be explained by positive selection, measurement by two methods (PALM indicated 12, MEME 61). Both evolutionary tests significantly marked sites 127, 731, 739, 766, and 780. SH2 is under evolutionary constraint but presents episodic positive selection events within Rodentia: in one of them, a moderately radical change (serine > arginine) at position 638 is found in Peromyscus species, and can be implicated in the difference in susceptibility to flaviviruses within Rodentia. Some other positively selected sites are functional such as 5, 95, 203, 251, 782, and 829. Sites 251 and 287 regulate the signaling mediated by the JAK-STAT2 pathway, while 782 and 829 create a stable tertiary structure of STAT2, facilitating its connection with transcriptional co-activators. Only three positively selected sites, 5, 95, and 203, are recognized members who act on the interface between STAT2 and flaviviruses NS5 protein. We suggested that due to the higher evolutionary rate, rodents are, at this moment, taking some advantage in the battle against infections for some well-known Flaviviridae, in particular when compared to primates. Our results point to dynamics that fit with a molecular evolutionary scenario shaped by a thought-provoking virus-host arms race.

A green racer snake (Philodryas nattereri, Colubridae) killed but not eaten by a blonde capuchin monkey (Sapajus flavius, Cebidae).

We report the killing of a snake (Philodryas nattereri, Colubridae) by a blonde capuchin monkey (Sapajus flavius, Cebidae). This endemic primate species from the northeast of Brazil includes vertebrates such as lizards and marsupials in its diet, but we can find no previously published record of an attack upon or consumption of snakes by this species of platyrhine monkey. During the attack, the group mobbed the snake, with individuals uttering agonistic vocalizations and displaying behaviors such as raising their tails, moving tree branches, piloerecting, and baring their teeth. An adult male monkey seized the snake, bit and twisted its body, thereby killing it; he then dropped the carcass onto tree branches, but did not consume it. This single event suggests that this Cebidae species may be able to distinguish dangerous from harmless snakes, and it also may be an example of a lethally violent reaction to a potential predator or competitor, exemplifying the plasticity and cognitive skills exhibited by genus Sapajus.

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.