Moving.

Examples of realized scientific careers can provide ideas and inspiration for others aiming to pursue such careers. Here I recount in brief the story of my long career in primatology (1973 to the present), focusing on one enduring theme in my research: the nature and genesis of goal-directed action (evident in movement). The story begins in graduate school, passes through developing my own laboratory, on to pursuing a spectrum of studies with mentees and collaborators, developing a theoretical explanatory framework for goal-directed action that I think holds promise for the field as a whole, and ends with an exciting field project that seems a suitable finale to my career. I mention the value to me, the field, and society of participation in scientific societies, including the American Society of Primatologists, throughout my career.

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.

Dexterity and technique in termite fishing by chimpanzees (Pan troglodytes troglodytes) in the Goualougo Triangle, Republic of Congo.

Although the phenomenon of termite fishing by chimpanzees (Pan troglodytes) has historical and theoretical importance for primatology, we still have a limited understanding of how chimpanzees accomplish this activity, and in particular, about details of skilled actions and the nature of individual variation in fishing techniques. We examined movements, hand positions, grips, and other details from remote video footage of seven adult and subadult female chimpanzees using plant probes to extract Macrotermes muelleri termites from epigeal nests. Six chimpanzees used exclusively one hand (left or right) to grip the probe during termite fishing. All chimpanzees used the same repertoire of actions to insert, adjust, and withdraw the probe but differed in the frequency of use of particular actions. Chimpanzees have been described as eating termites in two ways-directly from the probe or by sweeping them from the probe with one hand. We describe a third technique: sliding the probe between the digits of one stationary hand as the probe is extracted from the nest. The sliding technique requires complementary bimanual coordination (extracting with one hand and grasping lightly with the other, at the same time). We highlight the importance of actions with two hands-one gripping, one assisting-in termite fishing and discuss how probing techniques are correlated with performance. Additional research on digital function and on environmental, organismic, and task constraints will further reveal manual dexterity in termite fishing.

Compound grips in tufted capuchin monkeys (Sapajus spp and Sapajus libidinosus).

An experimental study with captive individuals and study of video recordings of wild monkeys explored whether and how tufted capuchin monkeys use onehand to hold one or more objects with multiple grips (compound grips). A task designed to elicit compound grip was presented to five captive tufted capuchin monkeys (Sapajus spp). The monkeys held one to four balls in onehand and dropped the balls individually into a vertical tube. Multiple simple grips and independent digit movements enabled separate control of multiple objects in one hand. Monkeys always supported the wrist on the horizontal edge of the tube before releasing the ball. Increasing the number of balls decreased the likelihood that the monkeys managed the task. Wild bearded capuchins (Sapajus libidinosus) used compound grips spontaneously to store multiple food items. Compound grips have been described in macaques, gorillas, chimpanzees, and humans, and now in a New World primate. We predict that any primate species that exhibits precision grips and independent digit movement can perform compound grips. Our findings suggest many aspects of compound grip that await investigation.

Adult and juvenile bearded capuchin monkeys handle stone hammers differently during nut-cracking.

Wild bearded capuchin monkeys (Sapajus libidinosus) habitually use stone hammers to crack open palm nuts and seeds on anvils. This activity requires strength, balance, and precise movement of a large stone with respect to the item placed on an anvil. We explored how well young monkeys cope with these challenges by examining their behavior and the behavior of adults while they cracked palm nuts using a stone. Using video records, we compared actions of six juvenile (2-5 years) and six adult (7+ years) wild monkeys during their first 20 strikes with one unfamiliar ellipsoid, quartzite stone (540 g), and the outcomes of these strikes. Compared with adults, juveniles cracked fewer nuts, performed a more diverse set of exploratory actions, and less frequently placed one or both hands on top of the stone on the downward motion. Adults and juveniles displayed similar low frequencies of striking with a slanted trajectory, missing the nut, and losing control over the nut or stone after striking. These findings indicate that young monkeys control the trajectory of a stone adequately but that is not sufficient to crack nuts as effectively as adults do. Compared with juveniles, adults more quickly perceive how to grip the stone efficiently, and they are able to adjust their grip dynamically during the strike. Young monkeys develop expertise in the latter aspects of cracking nuts over the course of several years of regular practice, indicating that perceptual learning about these aspects of percussion occurs slowly. Juvenile and adult humans learning to use stones to crack nuts also master these features of cracking nuts very slowly.

Synchronized practice helps bearded capuchin monkeys learn to extend attention while learning a tradition.

Culture extends biology in that the setting of development shapes the traditions that individuals learn, and over time, traditions evolve as occasional variations are learned by others. In humans, interactions with others impact the development of cognitive processes, such as sustained attention, that shape how individuals learn as well as what they learn. Thus, learning itself is impacted by culture. Here, we explore how social partners might shape the development of psychological processes impacting learning a tradition. We studied bearded capuchin monkeys learning a traditional tool-using skill, cracking nuts using stone hammers. Young monkeys practice components of cracking nuts with stones for years before achieving proficiency. We examined the time course of young monkeys' activity with nuts before, during, and following others' cracking nuts. Results demonstrate that the onset of others' cracking nuts immediately prompts young monkeys to start handling and percussing nuts, and they continue these activities while others are cracking. When others stop cracking nuts, young monkeys sustain the uncommon actions of percussing and striking nuts for shorter periods than the more common actions of handling nuts. We conclude that nut-cracking by adults can promote the development of sustained attention for the critical but less common actions that young monkeys must practice to learn this traditional skill. This work suggests that in nonhuman species, as in humans, socially specified settings of development impact learning processes as well as learning outcomes. Nonhumans, like humans, may be culturally variable learners.

Sense of ownership and not the sense of agency is spatially bounded within the space reachable with the unaugmented hand.

While reaching for a coffee cup, we are aware that the hand we see belongs to us and it moves at our will (reflecting our senses of ownership and agency, respectively), and that the cup is within our hand's reach rather than beyond it (i.e., in reachable space, RS, rather than in non-reachable space, NRS). Accepted psychological explanations of our sense of ownership, sense of agency, and our perception of space surrounding the body as RS or NRS propose a unitary dependence on Euclidean distance from the body. Here, we propose an alternate, affordance-based explanation of experienced ownership, agency, and perception of space surrounding the body as RS and NRS. Adult participants experienced the static rubber hand illusion (RHI) and its dynamic variant, while the rubber hand was either within their arm's reach (i.e., in self-identified RS) or beyond it (i.e., in self-identified NRS). We found that when the participants experienced synchronous visual and tactile signals in the static RHI, and synchronous visual and kinesthetic signals in the dynamic RHI, they felt illusory ownership when the rubber hand was in RS but not when it was in NRS. Conversely, when the participants experienced synchronous visual and kinesthetic signals in the dynamic RHI, they felt agency, regardless of the rubber hand's location. In addition, illusory ownership was accompanied by proprioceptive drift, a feeling that their hand was closer to the rubber hand than it actually was, but agency was not accompanied by proprioceptive drift. Together, these results indicate that our sense of ownership, while malleable enough to incorporate visible non-corporeal objects resembling a body part, is spatially constrained by proprioceptive signals specifying that body part's actual location. In contrast, our sense of agency can incorporate a visible non-corporeal object, independent of its location with respect to the body. We propose that the psychological processes mediating our sense of ownership are closely linked with our perception of space surrounding the body, and that the spatial independence of our sense of agency reflects the coupling between our actions and perception of the environment, such as while using handheld tools as extensions of our body.

Consistent inter-individual differences in susceptibility to bodily illusions.

Illusory senses of ownership and agency (that the hand or effector that we see belongs to us and moves at our will, respectively) support the embodiment of prosthetic limbs, tele-operated surgical devices, and human-machine interfaces. We exposed forty-eight individuals to four different procedures known to elicit illusory ownership or agency over a fake visible rubber hand or finger. The illusory ownership or agency arising from the hand correlated with that of the finger. For both body parts, sensory stimulation across different modalities (visual with tactile or visual with kinesthetic) produced illusions of similar strength. However, the strengths of the illusions of ownership and agency were unrelated within individuals, supporting the proposal that distinct neuropsychological processes underlie these two senses. Developing training programs to enhance susceptibility to illusions of agency or ownership for people with lower natural susceptibility could broaden the usefulness of the above technologies.

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.

How bearded capuchin monkeys (Sapajus libidinosus) prepare to use a stone to crack nuts.

Bearded capuchin monkeys crack nuts with naturally varying stone hammers, suggesting they may tune their grips and muscular forces to each stone. If so, they might use discrete actions on a stone before lifting and striking, and they would likely use these actions more frequently when the stone is larger and/or less familiar and/or when first initiating striking. We examined the behavior of (a) four monkeys (all proficient at cracking nuts) with two larger (1 kg) and two smaller (0.5 kg) stones, (b) 12 monkeys with one 1 kg stone, and (c) one monkey during its first 100 strikes with an initially unfamiliar 1 kg stone. Bearded capuchin monkeys used three discrete actions on the stone before striking, all more often with the larger stones than the smaller stones. We infer that the first discrete action (Spin) aided the monkey in determining where to grip the stone, the second (Flip) allowed it to position the stone on the anvil ergonomically before lifting it, and the third (Preparatory Lift) readied the monkey for the strenuous lifting action. The monkey that provided 100 strikes with one initially unfamiliar stone performed fewer Spins in later strikes but performed Flip and Preparatory Lift at consistent rates. The monkeys gripped the stone with both hands along the sides to lift it, but usually moved one or both hands to the top of the stone at the zenith of the lift for the downward strike. The findings highlight two new aspects of the capuchins' nut-cracking: (a) Anticipatory actions with the stone before striking, especially when the stone is larger or unfamiliar, and when initiating striking and (b) shifting grips on the stone during a strike. We invite researchers to investigate if other taxa use anticipatory actions and shift their grips during percussive activity.

Location of a grasped object's effector influences perception of the length of that object via dynamic touch.

Perception of properties of a grasped object via dynamic touch (wielding) contributes to dexterity in tool use (e.g., using a hammer, screwdriver) and sports (e.g., hockey, tennis). These activities differ from simple object manipulation in that they involve making contact with an intended target. In the present study, we examined whether and how making (percussive) contact with a target influences perception of the length of a grasped object via dynamic touch. Making contact with a target by the tip resulted in a more accurate perception of the length than simple wielding. However, making contact with the target at a point along the length did not influence the accuracy of perception. These findings suggest that the location of a grasped object's effector influences perception of properties of that object via dynamic touch. We discuss these findings in terms of time-varying properties of vibrations generated by the percussive contact of the grasped object and target.

Variations in an African Grey parrot's speech patterns following ignored and denied requests.

Communicative competence is one measure of an individual's ability to navigate conversations with social partners. The current study explored the possibility of basic communicative competence in a non-mammal speaker, a speech-using African Grey parrot. Spontaneous conversations between one Grey named Cosmo and her caregiver were recorded, from which three corpora (i.e., bodies of text) of Cosmo's vocalizations were developed: (1) Baseline: Vocalizations containing no requests, (2) Ignored Requests: Vocalizations immediately following Cosmo's caregiver ignoring Cosmo's requests, and (3) Denied Requests: Vocalizations immediately following Cosmo's caregiver denying Cosmo's requests. The distributions of social (e.g., "I love you," kiss sounds) and nonsocial (e.g., answering machine beeps, "That's squirrel") vocalizations, as well as speech and nonword vocalizations, were statistically different across the three corpora. Additionally, qualitative analysis of the datasets indicated Cosmo was persistent in repeating vocalizations when denied and ignored, and interrupted her caregiver more often when requests were denied compared to ignored. Neither repetition nor interruption occurred during the Baseline conversations. The data indicate that despite the outcome being the same (i.e., request was unmet), Cosmo treated an ignored request differently than a denied request, modifying her vocalizations in accord with the specific context. Such modification is evidence of basic communicative competence.

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

OBJECTIVES: 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. MATERIALS AND METHODS: 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. RESULTS: 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. DISCUSSION: 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.

Body mass in wild bearded capuchins, (Sapajus libidinosus): Ontogeny and sexual dimorphism.

Body mass is fundamental for understanding growth, health, and aspects of life history but records of body mass are rarely available for wild primates. We documented the body mass of all individuals in a group of wild bearded capuchin monkeys (Sapajus libidinosus) at annual intervals for seven consecutive years. Sexual dimorphism in body mass was more pronounced than reported in the literature for adults in this genus: females in our sample were relatively light (average 2.1 kg), while males had average body mass (3.5 kg). Three other notable differences between males and females were evident. First, males grew more rapidly and for a longer period than females. We estimate that males attained full body mass at 9.8 years of age and females at 7.5 years. Second, males showed greater inter-individual variability than females in growth rates and adult mass. Third, males gained about 20% above their baseline body mass upon becoming alpha, and lost that amount when they lost that status, but body mass in females was unrelated to social status. We also report preliminary data on mass and age of natal males at dispersal and mass and age at first reproduction for one female. The pattern of sexual dimorphism in ontogeny and inter-individual variability in body mass in bearded capuchins suggests different competitive risks in the two sexes commensurate with a mating system characterized by female choice of mates in multi-male, multi-female groups. Am. J. Primatol. 78:473-484, 2016. © 2015 Wiley Periodicals, Inc.

Does own experience affect perception of others' actions in capuchin monkeys (Cebus apella)?

Anticipating another's actions is an important ability in social animals. Recent research suggests that in human adults and infants one's own action experience facilitates understanding and anticipation of others' actions. We investigated the link between first-person experience and perception of another's action in adult tufted capuchin monkeys (Sapajus apella spp., formerly Cebus apella spp.). In Experiment 1, the monkeys observed a familiar human (actor) trying to open a container using either a familiar or an unfamiliar action. They looked for longer when the actor tried to open the container using a familiar action. In Experiment 2, the actor performed two novel actions on a new container. The monkeys looked equally at the two actions. In Experiment 3, the monkeys were trained to open the container using one of the novel actions in Experiment 2. After training, we repeated the same procedure as in Experiment 2. The monkeys looked for longer when the actor manipulated the container using the action they had practiced than when she used the unfamiliar action. These results show that knowledge derived from one's own experience impacts perception of another's action in these New World monkeys.

What limits tool use in nonhuman primates? Insights from tufted capuchin monkeys (Sapajus spp.) and chimpanzees (Pan troglodytes) aligning three-dimensional objects to a surface.

Perceptuomotor functions that support using hand tools can be examined in other manipulation tasks, such as alignment of objects to surfaces. We examined tufted capuchin monkeys' and chimpanzees' performance at aligning objects to surfaces while managing one or two spatial relations to do so. We presented six subjects of each species with a single stick to place into a groove, two sticks of equal length to place into two grooves, or two sticks joined as a T to place into a T-shaped groove. Tufted capuchins and chimpanzees performed equivalently on these tasks, aligning the straight stick to within 22.5° of parallel to the groove in approximately half of their attempts to place it, and taking more attempts to place the T stick than two straight sticks. The findings provide strong evidence that tufted capuchins and chimpanzees do not reliably align even one prominent axial feature of an object to a surface, and that managing two concurrent allocentric spatial relations in an alignment problem is significantly more challenging to them than managing two sequential relations. In contrast, humans from 2 years of age display very different perceptuomotor abilities in a similar task: they align sticks to a groove reliably on each attempt, and they readily manage two allocentric spatial relations concurrently. Limitations in aligning objects and in managing two or more relations at a time significantly constrain how nonhuman primates can use hand tools.

Multi-step routes of capuchin monkeys in a laser pointer traveling salesman task.

Prior studies have claimed that nonhuman primates plan their routes multiple steps in advance. However, a recent reexamination of multi-step route planning in nonhuman primates indicated that there is no evidence for planning more than one step ahead. We tested multi-step route planning in capuchin monkeys using a pointing device to "travel" to distal targets while stationary. This device enabled us to determine whether capuchins distinguish the spatial relationship between goals and themselves and spatial relationships between goals and the laser dot, allocentrically. In Experiment 1, two subjects were presented with identical food items in Near-Far (one item nearer to subject) and Equidistant (both items equidistant from subject) conditions with a laser dot visible between the items. Subjects moved the laser dot to the items using a joystick. In the Near-Far condition, one subject demonstrated a bias for items closest to self but the other subject chose efficiently. In the second experiment, subjects retrieved three food items in similar Near-Far and Equidistant arrangements. Both subjects preferred food items nearest the laser dot and showed no evidence of multi-step route planning. We conclude that these capuchins do not make choices on the basis of multi-step look ahead strategies.

The development of facial identity discrimination through learned attention.

Learned attention models of perceptual discrimination predict that with age, sensitivity will increase for dimensions of stimuli useful for discrimination. We tested this prediction by examining the face dimensions 4- to 6-month-olds (n = 77), 9- to 12-month-olds (n = 66), and adults (n = 73) use for discriminating human, monkey, and sheep faces systematically varying in outer features (contour), inner features (eyes, mouth), or configuration (feature spacing). We controlled interindividual variability across species by varying faces within natural ranges and measured stimulus variability using computational image similarity. We found the most improvement with age in human face discrimination, and older participants discriminated more species and used more facial properties for discrimination, consistent with learned attention models. Older infants and adults discriminated human, monkey, and sheep faces; however, they used different facial properties for primates and sheep. Learned attention models may provide insight into the mechanisms underlying perceptual narrowing.

How bipedalism shapes humans' actions with hand tools.

The task for an embodied cognitive understanding of humans' actions with tools is to elucidate how the human body, as a whole, supports the perception of affordances and dexterous action with objects in relation to other objects. Here, we focus on the relationship between humans' actions with handheld tools and bipedal posture. Posture plays a pivotal role in shaping animals' perception and action dynamics. While humans stand and locomote bipedally, other primates predominantly employ quadrupedal postures and locomotion, relying on both hands and feet to support the body. Drawing upon evidence from evolutionary biology, developmental psychology and performance studies, we elucidate the influence of bipedalism on our actions with objects and on our proficiency in using tools. We use the metaphor of cascades to capture the dynamic, nonlinear transformations in morphology and behaviour associated with posture and the use of tools across evolutionary and developmental timescales. Recent work illustrates the promise of multifractal cascade analysis to reveal nonlinear, cross-scale interactions across the entire body in real-time, supporting the perception of affordances for actions with tools. Cascade analysis enriches our comprehension of real-time performance and facilitates exploration of the relationships among whole-body coordination, individual development, and evolutionary processes.This article is part of the theme issue 'Minds in movement: embodied cognition in the age of artificial intelligence'.

Applying the bicoded spatial model to nonhuman primates in an arboreal multilayer environment.

Applying the framework proposed by Jeffery et al. to nonhuman primates moving in multilayer arboreal and terrestrial environments, we see that these animals must generate a mosaic of many bicoded spaces in order to move efficiently and safely through their habitat. Terrestrial light detection and ranging (LiDAR) technology and three-dimensional modelling of canopy movement may permit testing of Jeffery et al.'s framework in natural environments.