The use of probing tools by tufted capuchins (cebus apella): evidence for increased right-hand preference with age

We examined hand preference in the use of tools by tufted capuchins (Cebus apella). We presented a colony of monkeys with an enclosed container designed to accommodate the use of probing tools. Over an 8-month period, 13 monkeys used probes to extract sweet syrup from the narrow opening of the apparatus. Five monkeys exhibited bias toward use of their right hand and eight monkeys exhibited bias toward use of their left hand. Adult monkeys exhibited a greater percentage of right-hand preferent probing sequences than did juveniles. These results are consistent with hypotheses that in tasks that involve the use of tools, nonhuman primates exhibit strong lateral asymmetries at the individual level, a moderate left-hand bias at the population level, and increased bias with age toward use of the right hand.     

Hand preference in capuchin monkeys varies with age

The purpose of this research was to examine the influence of age on hand preference in capuchin monkeys (Cebus apella). Twenty-two capuchins, aged 6 months to 30 years, were presented with a task that involved reaching for food and a task that involved using sponging tools to absorb juice. Adults exhibited a greater percentage of right-handed actions in each task than did immature subjects. Adults also exhibited a stronger lateral bias than did immature subjects in the sponging task. These results are consistent with hypotheses: a) adult capuchin monkeys are biased toward use of their right hand for reaching; b) adult capuchins exhibit a greater incidence of right-hand preference than do immature capuchins; and c) primates exhibit age-related differences in the strength and direction of hand preference in tasks that involve the use of tools.     

Influence of the task on hand preference: individual differences among gorillas (Gorilla gorilla gorilla)

The degree of task complexity and bimanual complementarity have been proposed as factors affecting lateralization strength in humans. However, a large number of studies have demonstrated group-level lateral hand bias for different manual activities in numerous non-human primate species. However, no study has tested the effects that a variety of tasks may have in inducing differences in hand preference. Here, we aim to test if 3 adult gorillas exhibited a greater hand preference bias performing 4 tasks of varying complexity: grasping small versus large foods, proto-tool use task and tool use task involving greater visuospatial requirements. We found that (1) the complexity of the task does not necessarily induce a right-handed bias and (2) a subject can be right-handed for a complex task and left-handed for another one. These results, complemented by many publications on hand preference in non-human primates, reveal a great variability in hand preference, which makes it very difficult to deduce any details of hominin handedness with artefacts.     

Using the Tools at Hand: Manual Laterality and Elementary Technology in Cebus spp. and Pan spp.

Cebus and Pan appear to be a remarkable example of evolutionary convergence in behavioral ecology. We examine their apparently analogous solutions to problems posed by laterality of hand function and elementary technology. We scrutinize appropriate published data in a meta-analysis, focusing on Cebus apella and C. capucinus and on Pan paniscus and P. troglodytes. We compare behavioral data in terms of captive versus wild, and tool use versus non-tool use, but notable gaps exist in the data, especially for bonobos. Cebus and Pan spp. are equivalent tool users in captivity, but chimpanzees are notably more extensively so in nature. For hand preference, captive bonobos and wild and captive chimpanzees show ambipreference for non-tool-use patterns. For both Cebus spp. and Pan spp., there is a tendency for individuals to be committed exclusively to one hand or the other for tool use. The data for laterality of hand function fit consistently into the five-level model proposed by McGrew and Marchant (1996).     

Effects of upright posture on hand preference for reaching vs. the use of probing tools by tufted capuchins (Cebus apella)

This research examined the effects of task (reaching vs. Tool use) and posture (quadrupedal vs. bipedal) on hand preference in tufted capuchins (Cebus apella). Regarding direction of hand preference, we found a significant main effect of posture, as the bipedal stance elicited greater use of the right hand than did the quadrupedal stance, and a significant posture × task interaction, as bipedal reaching elicited greater use of the right hand than did other postural and task conditions. Further, we found a significant main effect of task on strength of hand preference, as tool use elicited more consistent use of one hand over the other than did reaching. Our findings indicate that bipedal reaching facilitates a mild right-hand bias in intensely manipulative primates. We speculate that this moderate bias may have been pushed in the direction of nearly exclusive right-hand preference in most humans with the development of complex tool use. Am. J. Primatol. 44:147–153, 1998. © 1998 Wiley-Liss, Inc. This article is a US Government work and, as such, is in the public domain in the United States of America.     

Manipulative Tendencies of Captive Cebus albifrons

We conducted two experiments to examine the manipulative tendencies of captive Cebus albifrons. In Experiment 1 we examined hand preference for reaching by providing subjects with food either on the cage floor (to facilitate quadrupedal reaching) or at the height of an upright subject's shoulder (to facilitate bipedal reaching). In Experiment 2 we examined combinatorial manipulation by providing subjects with nesting containers and other portable manipulanda. Results indicate that C. albifrons exhibits greater use of the right hand for bipedal versus quadrupedal reaching (exhibiting a group-level lack of bias for bipedal reaching and a left-hand bias for quadrupedal reaching), combines objects using a simple pairing strategy, and uses and produces simple tools. Aspects of these findings parallel those for Cebus apella.     

Hand preferences for a haptic searching task by tufted capuchins (Cebus apella)

We tested the effects of a haptic search task on hand preferences in capuchins(Cebus apella) and compare this situation to a visual by guided reaching task. In the haptic task, 21 monkeys searched for sunflower seeds on the top or side surfaces of 12 objects. A left-hand preference emerged at the group level, suggesting a greater involvement of the right hemisphere. The percentage of preferred hand usage and the direction of the preference were influenced by both sex and age of the subjects: adult males tended to be less lateralized than the other groups of subjects were. Shape had an insignificant effect on the direction of hand preferences or on the percentage of preferred hand use. No lateral bias emerge in the visually guided reaching task, and the percentage of left-hand usage fell significantly across tasks, demonstrating that the haptic demands of the task enhance the use of the left hand at the group level. We discuss these results with regard to current theories on manual lateralization in nonhuman primates.     

Oral tool use by captive orangutans (Pongo pygmaeus)

Eight captive orangutans (Pongo pygmaeus) were given wooden blocks embedded with raisins and bamboo as raw material for tool making in a study of manual laterality. In about three quarters of the raisin extraction bouts, the orangutans held the tool in the lips or teeth rather than in their hands. Three adult males and 2 adult females showed extreme (> or =92%) preference for oral tool use, a subadult male and an adult female used oral tools about half the time, and 1 adult female preferred manual tool use. Most oral tool users made short tools (approx. 4-10 cm long) that were held in the lips and (probably) supported by the tongue. Preference for oral tool use does not correlate with body weight, age or sex, but it may be related to hand size or individual preference. This is the first report of customary oral tool use as the norm in captive orangutans; it resembles the behavioral patterns reported by van Schaik et al. and Fox et al. in nature.     

Bipedal tool use strengthens chimpanzee hand preferences

The degree to which non-human primate behavior is lateralized, at either individual or population levels, remains controversial. We investigated the relationship between hand preference and posture during tool use in chimpanzees (Pan troglodytes) during bipedal tool use. We experimentally induced tool use in a supported bipedal posture, an unsupported bipedal posture, and a seated posture. Neither bipedal tool use nor these supported conditions have been previously evaluated in apes. The hypotheses tested were 1) bipedal posture will increase the strength of hand preference, and 2) a bipedal stance, without the use of one hand for support, will elicit a right hand preference. Results supported the first, but not the second hypothesis: bipedalism induced the subjects to become more lateralized, but not in any particular direction. Instead, it appears that subtle pre-existing lateral biases, to either the right or left, were emphasized with increasing postural demands. This result has interesting implications for theories of the evolution of tool use and bipedalism, as the combination of bipedalism and tool use may have helped drive extreme lateralization in modern humans, but cannot alone account for the preponderance of right-handedness.     

Ant fishing by wild chimpanzees is not lateralised

Right-dominant handedness is unique and universal in Homo sapiens, suggesting that it is a highly derived trait. Our nearest living relations, chimpanzees, show lateralised hand preference when using tools, but not when otherwise manipulating objects. We report the first contrary data, that is, non-lateralised tool-use, for ant fishing as done in the Mahale Mountains of Tanzania. Unlike nut cracking, termite fishing, and fruit pounding, as seen elsewhere, in which most individuals are either significantly or wholly left- or right-biassed, ant fishers are mostly ambilateral. The clue to this exception lies in arboreality; all other patterns of chimpanzee elementary technology are done on the ground. Arboreal tool use usually requires not only that one hand be used to hold the tool, but also that the other hand gives postural support. When the supporting hand is fatigued, then it must be relieved by the other. Terrestrial tool use entails no such trading off. To test the hypothesis, we compared frequency of hand changing with the incidence of major hand support, and found them to be significantly positively correlated. The evolutionary transition from arboreality to terrestriality may have been a key enabler for the origins of human laterality.     

Laterality in semi‐free‐ranging black and white ruffed lemurs (Varecia variegata variegata): head‐tilt correlates with hand use during feeding

Previous studies in human and chimpanzee infants have identified a predictive relationship between early rightward head orientation and later right hand use. Data from lemurs suggest a leftward bias in hand preference, but there are no data on head positioning. The purpose of this study was to examine the relationship between head and hand preferences in the black and white ruffed lemur (Varecia variegata variegata). Ruffed lemurs rotate the head vertically during chewing in a behavior called head‐tilting. Frequency of head‐tilting and bouts of unimanual hand use were measured during normal feeding in a semi‐free‐ranging population of lemurs. Subjects were provisioned at feeding platforms twice daily with fresh fruits, vegetables, and other food items. Sampling was spontaneous and all observations were videotaped. No group‐level bias was found for head‐tilting, but a left hand bias emerged for hand use. A positive relationship was found between direction of head‐tilting preference and direction of hand use preference such that left head‐tilts increased as left hand use increased. Furthermore, left head‐tilts increased as the degree of hand preference lateralization increased. When the hand used to bring food to the mouth just before head‐tilting was examined, there was a strong bias for the left hand to precede left head‐tilts. For right head‐tilts, however, lemurs were equally likely to use either hand before head‐tilting. Overall a strong relationship was found between the left hand and left head‐tilting in black and white ruffed lemurs, suggesting a common link between these behaviors. However, the direction of bias was different from that seen in human and chimpanzee studies. Additional studies on patterns of laterality would be informative for understanding how laterality has changed across the primate order and the adaptive significance of laterality in primates. Am. J. Primatol. 71:1032–1040, 2009. © 2009 Wiley‐Liss, Inc.     

Grasping behavior in tufted capuchin monkeys (Cebus apella): grip types and manual laterality for picking up a small food item

This study investigates prehension in 20 tufted capuchins (Cebus apella) in a reaching task requiring individuals to grasp a small food item fixed to a tray. The aim was twofold: 1) to describe capuchins' grasping techniques in detail, focusing on digit movements and on different areas of contact between the grasping fingers; and 2) to assess the relationship between grip types and manual laterality in this species. Capuchins picked up small food items using a wide variety of grips. In particular, 16 precision grip variants and 4 power grip variants were identified. The most frequently used precision grip involved the distal lateral areas of the thumb and the index finger, while the most preferred kind of power grip involved the thumb and the palm, with the thumb being enclosed by the other fingers. Immature capuchins picked up small food items using power grips more often than precision grips, while adult individuals exhibited no significant preference for either grip type. The analysis performed on the time capuchins took to grasp the food and withdraw it from the tray hole revealed that 1) precision grips were as efficient as power grips; 2) for precision grips, the left hand was faster than the right hand; and 3) for power grips, both hands were equally quick. Hand preference analysis, based on the frequency for the use of either hand for grasping actions, revealed no significant hand bias at group level. Likewise, there was no significant relationship between grip type and hand preference.     

Is Human Handedness Universal? Ethological Analyses from Three Traditional Cultures

Right-handedness in Homo sapiens is claimed to be qualitatively different from that of other primates, at species level, and to be universal across all cultures. Ethnographic indicators are sparse, however, being mostly indirect rather than direct observations of selected motor patterns. Ethological study of hand use, i.e. observation of a wide range of everyday behavioural patterns performed spontaneously, is missing. We coded such manual activity from cinematic archives of three traditional societies: G/wi San of Botswana, Himba of Namibia and Yanomamö of Venezuela. Results showed a consistent but weak right-hand dominance across these three preliterate cultures. Most individuals showed mixed-, rather than right-handedness, irrespective of whether or not object manipulation was involved. The notable exception was tool use, which was markedly right-handed, and only precision-gripping tool use was normally performed exclusively with the right hand. Most questionnaires that measure handedness focus on precision tool use (and so are likely to be biased accordingly) rather than on more comprehensive ethological measures that include non-object-manipulatory, self-directed and socially communicative patterns of behaviour.     

Hand Preferences in Different Tasks by Tufted Capuchins (Cebus apella)

We examined hand preferences in 25 tufted capuchins (Cebus apella) in three tasks. The hole task involved a single action of reaching for food in a hole. The horizontal panel and the vertical panel tasks required the alignment of two apertures, by moving or lifting a panel, to reach for food in a hole. We found a significant group-level right-hand preference for reaching actions in the hole and in the horizontal panel tasks, but not in the vertical panel task, in which the food retrieval implied the complementary use of both hands. No significant hand bias emerged for moving or lifting actions with high visuospatial components. There is a stronger hand preference in more complex manual activity—coordinated bimanual hand use for food retrieval—than in other unimanual measures. We discuss the results in the context of previous reports on primate laterality.     

Black lemur (Lemur macaco) hand preference in food reaching

The present study assessed the hand preferences exhibited by 33 black lemurs during routine feeding. Individual animals displayed hand preferences that were consistent across observations separated by as much as seven months. Within this population, 20 were left hand preferent, 12 right preferent, and 1 was ambidextrous. Correlational analysis of age and percentage left hand use indicated an inverse relationship in which younger animals tended towards the preferential use of the left hand and older animals the preferential use of the right hand. Similar analysis found no relationship between either sex and hand preference or familial relationship and hand preference. The skewed distribution of age in this sample renders tentative conclusions regarding age-related variations in hand preference. It is suggested that if the hand preferences of the black lemur are not age-related, then this species may be characterized as having a bias towards the preferential use of the left hand for food reaching.     

Lateralized tool use in wild New Caledonian crows

Many vertebrate species exhibit sensory and motor asymmetries. Laterality studies of tool use have focused on primates, where hemispheric asymmetries, manifested behaviourally in hand preferences, are thought to be associated with complex motor tasks. Here we report strong individual lateralization for tool use in birds. New Caledonian crows, Corvus moneduloides, hold stick tools with their bills while foraging, often with the nonworking end laterally positioned on one side of the head and the working end possibly positioned in the binocular field. We observed four wild crows to determine whether tools were consistently held on one side. All crows showed a significant preference (two right, two left). This preference was independent of any asymmetry in tool manufacture and held for artificial holes similarly accessible for tools held on either side. This is the first demonstration of lateralized tool use in a nonprimate. In addition, all 173 tools used unilaterally were held only on a crow's preferred side. Such pronounced individual laterality for tool use in natural conditions has previously been reported only in humans and chimpanzees.     

Hand preferences of captive chimpanzees (Pan troglodytes) in simple reaching for food

We examined chimpanzee hand preference in simple reaching for food, with special reference to manipulative patterns and the developmental shift. We observed 80 captive chimpanzees, ranging from 1 to 25 years old. We also studied the manipulative patterns (grip- types) of 70 individuals as they reached for raisins scattered randomly on the floor. We employed LQ score as a measure of hand preference and designated the subjects right- handers (or left- handers) if they used their right hands (left hands) above chance level. Although the numbers of right- handers and left- handers are almost equal, the distribution of the strength is not symmetrical in both groups. Strong preference was exhibited by more left- handers than right- handers. Subjects > 9 years old exhibited greater hand preference, whereas subjects < 9 years old were ambidextrous. We classified manipulative patterns for reaching into five basic grip- types and analyzed them vis- à- vis age. There is no significant correlation between preferred hand and manipulative patterns. However, adult subjects tended to use an index- and - middle- finger grip with the left hand and to use imprecise grips with the right hand more often than other patterns regardless which hand they preferred. These data demonstrate a developmental shift in hand preference and manipulative patterns and also reveal functional asymmetries between the right and the left hand in Pan troglodytes.     

Patterns of hand and mouth lateral biases in bamboo leaf shoot feeding and simple food reaching in the gentle lemur (Hapalemur griseus)

Lateralized feeding behaviors of 7 wild-born and 6 captive-born Hapalemur griseus sp. were evaluated in two conditions, simple food reaching and species-typical bamboo foraging. Gentle lemurs were found to have the strongest lateral hand preference in simple food reaching of any prosimian species yet studied. However in this small sample, population-level lateralization was not found: 5 preferred the right hand and 8 the left. The movement pattern used by hapalemurs when feeding on bamboo leaf shoots was categorized into four components: PULL IN, COUNTERFORCE, TURN, and FEED IN. Lateral hand bias was scored for all four components and lateral mouth preference was scored for the two components that involved the mouth (COUNTERFORCE and FEED IN). Strong positive correlations were found between hand preference in the most lateralized components of shoot eating (TURN and FEED IN) and simple food reaching. This suggests that the gentle lemurs' species-typical bamboo feeding behavior may contribute to the exceptionally strong hand preference for simple food reaching seen in this species. There were negative correlations between the component measure of shoot feeding that required strength (COUNTERFORCE) and the components that required manipulation (TURN and FEED IN). Within the COUNTERFORCE and FEED IN components, mouth preference and hand preference were positively associated in a manner that suggested one side of the mouth was preferred for removing the shoot and the other side for mastication. Asymmetrical dental wear may provide a means of dating behavioral lateralization in ancestral species. © 1993 Wiley-Liss, Inc.     

A multi-task assessment of hand lateralization in capuchin monkeys (Cebus apella)

Eight tasks were presented to ten tufted capuchin monkeys and hand preferences were recorded for each subject on each task. The strength of hand preferences varied accross tasks. Although no significant population-level left- or right-hand bias emerged for any of the tasks, there was a tendency toward greater left-hand use in a task requiring the use of probing tools. The data also confirm that simple reaching is of limited value as a measure of hand preference. Hand preferences in capuchin monkeys appear to be determined by a number of individual, species, and environmental factors.     

Lack of hand preference in wild Hanuman langurs (Presbytis entellus)

Although there is a vast literature on laterality of hand-use in nonhuman primates, the Colobinae have been notably overlooked. Ten manual activities of differing complexity were studied in five male and five female adult Hanuman langurs (Presbytis entellus) from a well habituated, wild population at Ramnagar, in southern Nepal. The activities recorded were carry, eat, hit, hold, idle, manipulate, reach, retrieve, self-groom and social groom. This study aimed to examine handedness across tasks and across subjects in a natural population. The overall result was a lack of preference for subjects and patterns. Only in the eating activity did four individuals show significant hand preference, though they were not unidirectional. Eat seemed to be loosely associated with hold due to the requirements of the strata which the monkeys utilize. These results suggest that hand use is unlateralized in P. entellus. Those individuals exhibiting some hand preferences can be viewed as statistical exceptions or perhaps subject to experiential differences. The results are discussed in terms of their evolutionary significance and methodological implications. Am J Phys Anthropol 103:455–461, 1997. © 1997 Wiley-Liss, Inc.