Wild Capuchin Research Articles

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 320km 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.

Female bearded capuchin monkeys (Sapajus libidinosus) use objects to solicit the sexual partner.

Female wild bearded capuchins (Sapajus libidinosus) living at Serra da Capivara National Park (SCNP) that use stone and stick tools during foraging occasionally toss or throw stones at the male during courtship. We report similar behaviors in a different population that uses stones as tools in foraging. We video-recorded the sexual behavior of four females (27 days during nine proceptive periods) belonging to a group of wild capuchins living in Fazenda Boa Vista (FBV), 320 km from SCNP. Three females used stones or branches when they solicited the alpha male (79 episodes). The female that did not use objects was the sole female to solicit a subordinate male. The vast majority of episodes (95%) involved pushing or dropping branches, both loose and attached to the tree, toward the male. Females used objects only during the one-way courtship phase, before the male reciprocated the female's solicitations. In 93% of the episodes in which a female used objects, she performed affiliative behaviors immediately before or after using the objects. We conclude that throwing or pounding stones and pushing or dropping branches by females in SCNP and FBV in the sexual context have a clear affiliative meaning (to attract the male's attention). Given the tool-using status of both populations where these behaviors have been reported, it is important to determine whether they appear in populations that do not use tools, or are restricted to populations already primed to use objects in other contexts. (PsycINFO Database Record

Older, sociable capuchins (Cebus capucinus) invent more social behaviors, but younger monkeys innovate more in other contexts

An important extension to our understanding of evolutionary processes has been the discovery of the roles that individual and social learning play in creating recurring phenotypes on which selection can act. Cultural change occurs chiefly through invention of new behavioral variants combined with social transmission of the novel behaviors to new practitioners. Therefore, understanding what makes some individuals more likely to innovate and/or transmit new behaviors is critical for creating realistic models of culture change. The difficulty in identifying what behaviors qualify as new in wild animal populations has inhibited researchers from understanding the characteristics of behavioral innovations and innovators. Here, we present the findings of a long-term, systematic study of innovation (10 y, 10 groups, and 234 individuals) in wild capuchin monkeys (Cebus capucinus) in Lomas Barbudal, Costa Rica. Our methodology explicitly seeks novel behaviors, requiring their absence during the first 5 y of the study to qualify as novel in the second 5 y of the study. Only about 20% of 187 innovations identified were retained in innovators’ individual behavioral repertoires, and 22% were subsequently seen in other group members. Older, more social monkeys were more likely to invent new forms of social interaction, whereas younger monkeys were more likely to innovate in other behavioral domains (foraging, investigative, and self-directed behaviors). Sex and rank had little effect on innovative tendencies. Relative to apes, capuchins devote more of their innovations repertoire to investigative behaviors and social bonding behaviors and less to foraging and comfort behaviors.

Wild capuchin monkeys anticipate the amount of ripe fruit in natural trees.

Tropical forests have a high diversity of tree species which have very low densities and vary across time in their seasons of peak fruiting and maturation rates. As evidence of the ability of primates to track or anticipate changes in fruit production at individual trees, researchers have used the increased speed of primate groups toward more rewarding food patches. We analyzed the speed of approach to natural trees of wild capuchin monkeys under the effect of scramble competition, after excluding any plausible visual, olfactory and auditory cues. We conducted all-day group follows of three habituated capuchin groups at Iguazú National Park, Argentina, collecting data on ranging behavior and patterns of visits to fruit trees in relation with their location and fruit availability. Travel speed varied according to the expected reward at a feeding tree, increasing as rewards increased from low values, but decreasing again at very high values. Also, travel speed varied with time of day, decreasing from the time of first activity as the monkeys became less hungry, and increasing again toward late afternoon. Measures of unripe fruit cover did not explain variation in travel speed at any distance from a focal tree. Our data imply that, after excluding sensory cues, capuchins appear to anticipate time-varying ripe fruit quantity of natural resources, suggesting that they use memory of tree location and anticipation of fruit maturation. We also confirm that speed is a good measure about expectations of resources, as has been shown in previous studies.

Whose Tools Are These?

The article discusses the archaeological discovery of stone flake tools developed by wild capuchin monkeys in Serra da Capivara National Park in northeastern Brazil, referencing a study co-authored by scientist Tomos Proffitt in the journal "Nature." The relationship between prehistoric human tools and the tools created by capuchin monkeys, including in regard to Oldowan tools, is discussed.

Capuchins, space, time and memory: an experimental test of what-where-when memory in wild monkeys.

There is considerable controversy about the existence, extent and adaptive value of integrated multimodal memory in non-human animals. Building on prior results showing that wild capuchin monkeys in Argentina appear to recall both the location and amount of food at patches they had previously visited, I tested whether they also track and use elapsed time as a basis for decisions about which feeding patches to visit. I presented them with an experimental array of eight feeding sites, at each of which food rewards increased with increasing elapsed time since the previous visit, similar to the pattern of ripe fruit accumulation in natural feeding trees. Over the course of 68 days, comprising two distinct renewal rate treatments, one group repeatedly visited sites in the feeding array, generating 212 valid choices between sites. Comparison of observations against simulated movements and multinomial statistical models shows that the monkeys' choices were most consistent with dynamic memory for elapsed time specific to each of the eight sites. Thus, it appears that capuchin monkeys possess and use integrated memories of prior food patch use, including where the patch is relative to their current location, how productive the patch is and how long it has been since they last visited the patch. Natural selection to use such integrated memories in foraging tasks may provide an ecologically relevant basis for the evolution of complex intelligence in primates.

Wild capuchin monkeys adjust stone tools according to changing nut properties.

Animals foraging in their natural environments need to be proficient at recognizing and responding to changes in food targets that affect accessibility or pose a risk. Wild bearded capuchin monkeys (Sapajus libidinosus) use stone tools to access a variety of nut species, including otherwise inaccessible foods. This study tests whether wild capuchins from Serra da Capivara National Park in Brazil adjust their tool selection when processing cashew (Anacardium spp.) nuts. During the ripening process of cashew nuts, the amount of caustic defensive substance in the nut mesocarp decreases. We conducted field experiments to test whether capuchins adapt their stone hammer selection to changing properties of the target nut, using stones of different weights and two maturation stages of cashew nuts. The results show that although fresh nuts are easier to crack, capuchin monkeys used larger stone tools to open them, which may help the monkeys avoid contact with the caustic hazard in fresh nuts. We demonstrate that capuchin monkeys are actively able to distinguish between the maturation stages within one nut species, and to adapt their foraging behaviour accordingly.

Wild capuchin monkeys spontaneously adjust actions when using hammer stones of different mass to crack nuts of different resistance.

Expert tool users are known to adjust their actions skillfully depending on aspects of tool type and task. We examined if bearded capuchin monkeys cracking nuts with stones of different mass adjusted the downward velocity and the height of the stone when striking palm nuts. During a field experiment carried out in FBV (Piauí, Brazil), eight adult wild capuchin monkeys (five males) cracked Orbygnia nuts of varied resistance with hammer stones differing in mass. From recorded videos, we identified the highest strike per nut-cracking episode, and for this strike, we calculated the height to which the monkey lifted the stone, the maximum velocity of the stone during the downward phase, the work done on the stone, and the kinetic energy of the strike. We found that individual capuchins achieved average maximum kinetic energy of 8.7-16.1 J when using stones between 0.9 and 1.9 kg, and maximum kinetic energy correlated positively with mass of the stone. Monkeys lifted all the stones to an individually consistent maximum height but added more work to the stone when using lighter stones. One male and one female monkey lifted stones higher when they cracked more resistant nuts. The high resistance of the Orbygnia nut elicits production of maximum kinetic energy, which the monkeys modulate to some degree by adding work to lighter stones. Capuchin monkeys, like chimpanzees, modulate their actions in nut-cracking, indicating skilled action, although neither species regulates kinetic energy as precisely as skilled human stone knappers. Kinematic analyses promise to yield new insights into the ways and extent to which nonhuman tool users develop expertise. Am J Phys Anthropol 161:53-61, 2016. © 2016 Wiley Periodicals, Inc.

Cues to kinship and close relatedness during infancy in white-faced capuchin monkeys, Cebus capucinus

The ability to recognize kin has important impacts on fitness because it can allow for kin-biased affiliative behaviours and avoidance of mating with close kin. While the presence and effects of kin biases have been widely studied, less is known about the process by which animals recognize close kin. Here we investigate potential cues that white-faced capuchin monkeys, Cebus capucinus, may use to detect half siblings and closer kin. We focus on the first year of life in a sample of 130 infant (N = 65 infant females) wild capuchins from the Lomas Barbudal population in Costa Rica. We show that (1) infant relatedness to juvenile and adult males at the level of half sibling and higher can be predicted by male alpha status, spatial proximity and age proximity, and that (2) infant relatedness to juvenile and adult females at the level of half sibling or higher can be predicted by spatial proximity (but not age proximity). Furthermore, (1) the identities of infants' fathers can also be predicted by male alpha status and the spatial proximity between infants and adult males, and (2) age proximity (but not spatial proximity) is predictive of paternal sibship. These results suggest that infant capuchins have access to multiple cues to close relatedness and paternal kinship, although whether infants use these cues later in life remains to be explored in future research.

When and where to practice: social influences on the development of nut-cracking in bearded capuchins (Sapajus libidinosus).

The habitual use of tools by wild capuchin monkeys presents a unique opportunity to study the maintenance and transmission of traditions. Young capuchins spend several years interacting with nuts before cracking them efficiently with stone tools. Using a two-observer method, we quantified the magnitude of the social influences that sustain this long period of practice. During five collection periods (over 26 months), one observer recorded the behavior of 16 immature monkeys, and another observer concurrently recorded behavior of group members in the focal monkey's vicinity. The two-observer method provides a means to quantify distinct social influences. Data show that immatures match the behavior of the adults in time and especially in space. The rate of manipulation of nuts by the immatures quadrupled when others in the group cracked and ate nuts, and immatures were ten times more likely to handle nuts and 40 times more likely to strike a nut with a stone when they themselves were near the anvils. Moreover, immature monkeys were three times more likely to be near an anvil when others were cracking. We suggest a model for social influence on nut-cracking development, based on two related processes: (1) social facilitation from observing group members engaged in nut-cracking, and (2) opportunity for practice provided by the anvils, hammer stones and nut shells available on and around the anvils. Nut-cracking activities by others support learning by drawing immatures to the anvils, where extended practice can take place, and by providing materials for practice at these places.

The strategic role of the tail in maintaining balance while carrying a load bipedally in wild capuchins (Sapajus libidinosus): a pilot study.

The ability to carry objects has been considered an important selective pressure favoring the evolution of bipedal locomotion in early hominins. Comparable behaviors by extant primates have been studied very little, as few primates habitually carry objects bipedally. However, wild bearded capuchins living at Fazenda Boa Vista spontaneously and habitually transport stone tools by walking bipedally, allowing us to examine the characteristics of bipedal locomotion during object transport by a generalized primate. In this pilot study, we investigated the mechanical aspects of position and velocity of the center of mass, trunk inclination, and forelimb postures, and the torque of the forces applied on each anatomical segment in wild bearded capuchin monkeys during the transport of objects, with particular attention to the tail and its role in balancing the body. Our results indicate that body mass strongly affects the posture of transport and that capuchins are able to carry heavy loads bipedally with a bent-hip-bent-knee posture, thanks to the "strategic" use of their extendable tail; in fact, without this anatomical structure, constituting only 5% of their body mass, they would be unable to transport the loads that they habitually carry.

Making use of capuchins’ behavioral propensities to obtain hair samples for DNA analyses


 
 
 Genotyping wild and captive capuchins has become a priority and hair bulbs have high quality DNA. Here, we describe a method to non-invasively collect fresh-plucked strands of hair that exploits capuchins’ manual dexterity and propensity to grasp and extract food. The apparatus consists of a transparent tube baited with food. Its extraction requires the monkey to place its forearm in contact with double-sided tape applied on the inner surface of the tube entrance. The “tube” method, successfully implemented with captive (N=23) and wild (N=21) capuchins, allowed us to obtain hair bulbs from most indi- viduals and usable genomic DNA was extracted even from a single bulb.
 
 

Nasal probe and toothpick tool use by a wild female bearded capuchin (Sapajus libidinosus).

We report the first observation of probe tool use by a wild adult female bearded capuchin (Sapajus libidniosus), at Serra da Capivara National Park (SCNP), Brazil. This individual used several stick tools and one grass stem to probe her nostrils, usually triggering a sneeze reaction, and also used stick tools to probe her teeth or gum. Both of these behaviours were accompanied by inspection and licking of the tool following use. We have termed these self-directed actions nasal probe and toothpick, and neither has been previously reported in wild capuchins. While stick tool use is common among foraging male capuchins at SCNP, the novel and at present idiosyncratic activities performed by the female monkey add to the known behavioural repertoire for this species.Electronic supplementary materialThe online version of this article (doi:10.1007/s10329-015-0470-6) contains supplementary material, which is available to authorized users.

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.

Adaptability in stone tool use by wild capuchin monkeys (Sapajus libidinosus)

Capuchin monkeys are well known for population variation in the use of stone tools and the types of food items consumed. In order to determine adaptability in stone tool use, we investigated a never before studied population of wild capuchin monkey (Sapajus libidinosus) displaying terrestrial habits in a Caatinga environment. To carry out this study we recorded physical evidence of the use of stone tools as well as made direct observations through trap cameras. During a 15-month period, we studied a group of Sapajus libidinosus in Serra Talhada, Pernambuco, Brazil. In total, 257 anvils and 395 hammers were identified, characterized, and monitored. We identified five types of food items exploited at these "tool use sites": Syagrus oleracea (catolé palm), Manihot epruinosa (manioc), Pilosocereus pachycladus (facheiro), Tacinga inamoena (quípa), and Commiphora leptophloeos (imburana de cambão). Five hundred three video clips of capuchin monkeys were recorded, 43 of which involved the use of stone tools. The results indicated evidence of adaptability in tool use by the capuchins. We verified that the rigidity and size of the food item, along with the presence or absence of spines seem to influence the choice of stone tools made by the animals for processing the food. The recurring use of tools for the processing of cacti was especially noteworthy and it appears that the presence of spines predisposes the capuchins to use stones to process them. A significant difference was observed between the characteristics of the anvils and the weight of the hammers according to the food item consumed. The use of tools enabled the animals to access otherwise unavailable or difficult to acquire food items within a Caatinga habitat. Adaptability in the use of stone tools by the capuchin monkey population of Serra Talhada provides an example of the complexity that these primates demonstrate in food processing.

Seasonality, extractive foraging and the evolution of primate sensorimotor intelligence

The parallel evolution of increased sensorimotor intelligence in humans and capuchins has been linked to the cognitive and manual demands of seasonal extractive faunivory. This hypothesis is attractive on theoretical grounds, but it has eluded widespread acceptance due to lack of empirical data. For instance, the effects of seasonality on the extractive foraging behaviors of capuchins are largely unknown. Here we report foraging observations on four groups of wild capuchins (Cebus capucinus) inhabiting a seasonally dry tropical forest. We also measured intra-annual variation in temperature, rainfall, and food abundance. We found that the exploitation of embedded or mechanically protected invertebrates was concentrated during periods of fruit scarcity. Such a pattern suggests that embedded insects are best characterized as a fallback food for capuchins. We discuss the implications of seasonal extractive faunivory for the evolution of sensorimotor intelligence (SMI) in capuchins and hominins and suggest that the suite of features associated with SMI, including increased manual dexterity, tool use, and innovative problem solving are cognitive adaptations among frugivores that fall back seasonally on extractable foods. The selective pressures acting on SMI are predicted to be strongest among primates living in the most seasonal environments. This model is proffered to explain the differences in tool use between capuchin lineages, and SMI as an adaptation to extractive foraging is suggested to play an important role in hominin evolution.

The heterozygote superiority hypothesis for polymorphic color vision is not supported by long-term fitness data from wild neotropical monkeys.

The leading explanatory model for the widespread occurrence of color vision polymorphism in Neotropical primates is the heterozygote superiority hypothesis, which postulates that trichromatic individuals have a fitness advantage over other phenotypes because redgreen chromatic discrimination is useful for foraging, social signaling, or predator detection. Alternative explanatory models predict that dichromatic and trichromatic phenotypes are each suited to distinct tasks. To conclusively evaluate these models, one must determine whether proposed visual advantages translate into differential fitness of trichromatic and dichromatic individuals. We tested whether color vision phenotype is a significant predictor of female fitness in a population of wild capuchins, using longterm 26 years survival and fertility data. We found no advantage to trichromats over dichromats for three fitness measures fertility rates, offspring survival and maternal survival. This finding suggests that a selective mechanism other than heterozygote advantage is operating to maintain the color vision polymorphism. We propose that attention be directed to field testing the alternative mechanisms of balancing selection proposed to explain opsin polymorphism nichedivergence, frequencydependence and mutual benefit of association. This is the first indepth, longterm study examining the effects of color vision variation on survival and reproductive success in a naturallyoccurring population of primates.

The Behavioral Ecology of Color Vision: Considering Fruit Conspicuity, Detection Distance and Dietary Importance

Primate color vision is well suited for investigating the genetic basis of foraging behavior owing to a clear genotype–phenotype linkage. Finding fruits amid tropical foliage has long been proffered as an adaptive explanation for primate trichromacy, yet there is a dearth of systematic evaluations of frugivory as an ecological selective force. We studied the behavioral ecology of wild capuchins (Cebus capucinus) in northwestern Costa Rica across the annual cycle and modeled the ability of three dichromatic and three trichromatic phenotypes to discriminate fruits from leaves, a task that represents long-distance search for food patches in a tropical forest. Models of the trichromatic phenotypes could correctly discriminate approximately three-quarters of the total capuchin dietary fruits from leaves, including some fruits subjectively classified as having “cryptic” (greenish-brownish) hues. In contrast, models of dichromatic phenotypes could discriminate fewer than one-third of the fruits. This pattern held when we restricted our analysis to only the most heavily consumed diet items, preferred foods, or seasonally critical species. We in addition highlight the potential of fruit species with small patch sizes to confer an advantage to trichromats, as these resources are anticipated to provide a high finder’s reward. Our results are consistent with the hypothesis that long-distance detection of fruit patches exerts a selective pressure on trichromacy in neotropical primates, and suggest that greenish-brownish fruits might have played an underappreciated role in the evolution of primate color vision.

Predictors of Parasitism in Wild White-Faced Capuchins (Cebus capucinus)

Parasite infections in wildlife are influenced by many factors including host demography, behavior and physiology, climate, habitat characteristics, and parasite biology and ecology. White-faced capuchins (Cebus capucinus) host a suite of gastrointestinal and pulmonary parasites, yet the mechanisms affecting host susceptibility and parasite transmissibility have not been examined in this host species. We used the information-theoretic approach (Akaike's information criterion) and traditional null-hypothesis testing to determine which host characteristics, behaviors, or environmental factors affected the presence of two prevalent capuchin parasites (Filariopsis barretoi and Strongyloides sp.) as well as parasite species richness in four groups of wild capuchins from September 2007 to January 2008 and January to August 2009. Older capuchins were more likely to be infected with Filariopsis barretoi and had higher parasite species richness. Age-biased nematode infections may stem from age differences in capuchin behavior and physiology while high species richness likely results from long- term exposure to numerous parasite species. Infections with Strongyloides sp. were more likely to occur in the dry season when capuchins often descend to the forest floor to drink from terrestrial water sources, potentially increasing their risk of infection from soil-borne larvae. Capuchin behaviors were poor predictors of parasitism, as were female rank, host sex, home range size, and habitat quality. Many of our results were atypical for primate parasitology, suggesting that host-parasite interactions, and subsequently infection risk, may differ in highly seasonal habitats such as tropical dry forests where these monkeys occur.

Archaeology meets primate technology

A study of wild capuchin monkeys that crack nuts using stone hammers reveals temporal and spatial patterning of the relics of their technological efforts, confirming that such behaviours can be studied from an archaeological perspective.