Anticipating future actions: Motor planning improves with age in wild bearded capuchin monkeys (Sapajus libidinosus).

Self-directed object manipulation tasks illuminate development of motor planning. Grasping strategies that lead to good object control to perform the following action(s) reveal second-order motor planning. Motor planning for efficient grips develops slowly in children. Age-related differences in other primates have been poorly investigated. Here, we investigated anticipatory motor planning of infant, juvenile and adult wild capuchin monkeys grasping a horizontally positioned stick baited to the left or right side (a version of the elevated spoon task). We recorded the grasps capuchins used to bring the baited end of the stick to the mouth. The percentage of efficient radial grips positively correlated with age and adults used efficient grips significantly more frequently than infants. Adult wild capuchins' use of radial grips was higher than that reported for adult captive capuchins in similar tasks, suggesting that experience throughout life may influence motor anticipation. Self-directed object manipulation tasks will be useful to compare this aspect of cognition across primates. A video abstract of this article can be viewed at https://youtu.be/a1Zbr_AQkb8.

Manual skills for processing plant underground storage organs by wild bearded capuchins.

OBJECTIVES: Wild Sapajus libidinosus exploit underground storage organs (USOs) that require extraction and extensive processing before consumption. Since capuchin monkeys are small-sized extractive foragers that cannot perform forceful precision grips, we expected that: (a) they would use other body parts together with their hands, (b) older (and larger) capuchins would be more efficient than younger (and smaller) ones, and (c) capuchins would invest greater effort/time to exploit USOs than other foods. MATERIALS AND METHODS: We recorded 178 episodes of USO processing performed by 20 individuals. The behavior was videotaped and scored frame-by-frame. RESULTS: We identified six sequential stages of processing: Excavation, extraction, soil removal, transport, peeling, and fragmenting the inner tissues. Capuchins made frequent use of forceful hand postures and manipulation in which the hands were strongly supported by other body parts, principally the mouth. Older capuchins were more efficient than younger individuals in pulling the USOs out of the ground. Finally, exploiting USOs was time-consuming, lasting more than 4 min per item, on average. DISCUSSION: Despite having smaller body-mass and greater manual constraints than catarrhine extractive foragers, capuchins, even smaller individuals, mastered USO processing thanks to their behavioral flexibility and persistence. Our findings reveal that precision grips are not essential for forceful actions during complex food processing and that, unlike catarrhines, capuchins, especially adults, rarely use thumb opposition during forceful grasping of food. In contrast, extended sustained attention and varied manual behavior appear to be convergent features of platyrrhine and catarrhine extractive foragers.

Factors affecting cashew processing by wild bearded capuchin monkeys (Sapajus libidinosus, Kerr 1792).

Cashew nuts are very nutritious but so well defended by caustic chemicals that very few species eat them. We investigated how wild bearded capuchin monkeys (Sapajus libidinosus) living at Fazenda Boa Vista (FBV; Piauí, Brazil) process cashew nuts (Anacardium spp.) to avoid the caustic chemicals contained in the seed mesocarp. We recorded the behavior of 23 individuals toward fresh (N = 1282) and dry (N = 477) cashew nuts. Adult capuchins used different sets of behaviors to process nuts: rubbing for fresh nuts and tool use for dry nuts. Moreover, adults succeed to open dry nuts both by using teeth and tools. Age and body mass significantly affected success. Signs of discomfort (e.g., chemical burns, drooling) were rare. Young capuchins do not frequently closely observe adults processing cashew nuts, nor eat bits of nut processed by others. Thus, observing the behavior of skillful group members does not seem important for learning how to process cashew nuts, although being together with group members eating cashews is likely to facilitate interest toward nuts and their inclusion into the diet. These findings differ from those obtained when capuchins crack palm nuts, where observations of others cracking nuts and encounters with the artifacts of cracking produced by others are common and support young individuals' persistent practice at cracking. Cashew nut processing by capuchins in FBV appears to differ from that observed in a conspecific population living 320 km apart, where capuchins use tools to open both fresh and dry nuts. Moreover, in the latter population, chemical burns due to cashew caustic compounds appear to be common. The sources of these differences across populations deserve investigation, especially given that social influences on young monkeys learning to open cashew nuts at FBV seem to be nonspecific. Am. J. Primatol. 78:799-815, 2016. © 2016 Wiley Periodicals, Inc.

Ingestive behaviors in bearded capuchins (Sapajus libidinosus).

The biomechanical and adaptive significance of variation in craniodental and mandibular morphology in fossil hominins is not always clear, at least in part because of a poor understanding of how different feeding behaviors impact feeding system design (form-function relationships). While laboratory studies suggest that ingestive behaviors produce variable loading, stress, and strain regimes in the cranium and mandible, understanding the relative importance of these behaviors for feeding system design requires data on their use in wild populations. Here we assess the frequencies and durations of manual, ingestive, and masticatory behaviors from more than 1400 observations of feeding behaviors video-recorded in a wild population of bearded capuchins (Sapajus libidinosus) at Fazenda Boa Vista in Piauí, Brazil. Our results suggest that ingestive behaviors in wild Sapajus libidinosus were used for a range of food material properties and typically performed using the anterior dentition. Coupled with previous laboratory work indicating that ingestive behaviors are associated with higher mandibular strain magnitudes than mastication, these results suggest that ingestive behaviors may play an important role in craniodental and mandibular design in capuchins and may be reflected in robust adaptations in fossil hominins.

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.