Consistency of hand preference across low-level and high-level tasks in capuchin monkeys (Cebus apella)

Numerous studies investigating behavioral lateralization in capuchins have been published. Although some research groups have reported a population-level hand preference, other researchers have argued that capuchins do not show hand preference at the population level. As task complexity influences the expression of handedness in other primate species, the purpose of this study was to collect hand preference data across a variety of high- and low-level tasks to evaluate how task complexity influences the expression of hand preference in capuchins. We tested eleven captive brown capuchin monkeys (Cebus apella) to determine if they show consistent hand preferences across multiple high- and low-level tasks. Capuchins were expected to display high intertask consistency across the high-level tasks but not the low-level tasks. Although most individuals showed significant hand preferences for each task, only two of the high-level tasks that involved similar hand motions were significantly positively correlated, indicating consistency of hand preference across these tasks only. None of the tasks elicited a group-level hand preference. High-level tasks elicited a greater strength of hand preference than did low-level tasks. No sex differences were found for the direction or strength of hand preference for any task. These results contribute to the growing database of primate laterality and provide additional evidence that capuchins do not display group-level hand preferences.     

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.     

Hand preference in a captive island group of chimpanzees (Pan troglodytes)

Morphological cerebral asymmetries in chimpanzee brains, similar to those found in humans, in whom they are associated with speech and handedness, suggest the possibility of functional lateralization in the chimpanzee. This possibility was investigated by examining hand preferences in an island group of five chimpanzees on a series of unimanual and bimanual tasks that are diagnostic of human hand and cerebral dominance. Each subject was tested in a double compartment cage on three unimanual nonsequential, three unimanual sequential, and three bimanual coordination tasks. One of the three unimanual sequential tasks was a bar-press task that is analogous to the commonly used human finger-tapping task. For the unimanual tasks, exclusive of the bar-press, the chimpanzees showed a highly individualistic pattern of hand preference that did not change as a function of task complexity. On the bar-press task, four of five subjects produced higher rates with one hand compared to the other; however, relative hand performance on this task was unrelated to hand preference on the other unimanual tasks. For the group of subjects, performance rates did not differ between the left and right hands; however, a practice effect was observed for the right hand in all subjects. The bimanual tasks also revealed a complex pattern of individual handedness, with no trends apparent for the group as a whole. Consistent with previous findings, the results from these tests on this group of five chimpanzees suggest that cerebral morphological asymmetries in the chimpanzee are not associated with motor dominance as reflected in handedness.     

Sex difference in chimpanzee handedness

Chimpanzees at Mahale, Tanzania, show strong individual hand preferences when they use bimanual actions in processing the fruit of Saba florida and Citrus lemon. The direction of hand preference differs between the sexes: most males are left-handed, whereas most females are right-handed. Monkeys and apes are considered to lack "handedness," in the sense of a population mode of left- or right-hand preference; they are normally ambidextrous. Indeed, strong individual preferences were previously seldom found in natural tasks. We propose that lateralization of manual actions becomes advantageous in bimanual tasks, which involve role differentiation between the hands and a need to combine power and precision. If the pattern of lateralization found here reflects the ancestral state, common to chimpanzees and humans, this may explain why, in modern humans, women tend more strongly to be right-handed than men, who include a larger minority of left-handers.     

Does the Complexity of the Task Influence Manual Laterality in De Brazza’s Monkeys (Cercopithecus neglectus)?

We assessed the manual preferences of 12 De Brazza's monkeys ( Cercopithecus neglectus ) in spontaneous feeding situations and in two different coordinated bimanual tasks that were not visually guided. We recorded the hand used by each subject for 22 spontaneous activities, hand and digits use while extracting peanut butter from a hollow tube (tube task) and the hand used to extract candies from hanging plastic balls (ball task). Spontaneous activities revealed individual manual preferences but no population-level biases. For both experimental tasks, all subjects were lateralized in their hand use. We found a left bias at the group level for the tube task, but no group-level asymmetry for the ball task. Experimental tasks induced greater strength of laterality than did spontaneous activities. Although the size of our sample did not allow us to draw any conclusions concerning manual preference at the population level, this study stresses the importance of coordinated bimanual tasks to reveal manual laterality in non-human primates.     

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.     

Manual Laterality for Simple Reaching and Bimanual Coordinated Task in Naturalistic Housed <Emphasis Type="Italic">Pan troglodytes</Emphasis>

Researchers have shown renewed interest in the study of manual lateralization in chimpanzees. Currently there is no consensus confirming the presence or absence of manual dominance at a species level, mainly for populations in the wild and in semicaptivity. We aimed to evaluate the manual laterality in a group of chimpanzees in an intermediate setting (semicaptivity) via 2 tasks: one simple and unimanual (simple reaching) and the other complex and bimanual (tube task). We replicated the same experiments from Hopkins in a new and different sample of chimpanzees. In simple reaching, the hand is used to gather food and the type of grip and the posture are evaluated. The tube task assesses the hand used to extract food from the tube and the method of extraction (digital or instrumental). Through the handedness index we observed that the subjects show clear and strong individual preferences for both tasks (100% lateralized subjects in the tube task; 86% in simple reaching), although we did not detect population preferences for any of the tasks. However, considering both tasks jointly (multiple evaluation), it was possible to detect, for the first time, skilled manual dominance at a group level in semicaptive chimpanzees in one multitask index and borderline significance in a second multitask index.     

Factor Analysis of Multiple Measures of Hand Use in Captive Chimpanzees: An Alternative Approach to the Assessment of Handedness in Nonhuman Primates

We tested whether chimpanzee handedness could be characterized as either unidimensional or multidimensional when considered across multiple measures of hand use. We determined for each of 6 different tasks in a sample of 105 captive chimpanzees hand preferences, and subjected the individual hand preference scores to a factor analysis. Five of the 6 tasks loaded on two separate factors that accounted for 54% of the variance. To assess population-level handedness, we calculated handedness indices for the loadings on each factor, for the item loadings across all factors, and for all tasks including ones that did not load on any factor. There is significant population-level right handedness for all 4 indices, which suggests that chimpanzee handedness is multidimensional and not task specific.     

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.     

Principles and levels of laterality in unimanual and bimanual stone handling patterns by Japanese macaques

The preferential use of one hand over the other is considered the primary behavioral expression of structural and functional asymmetry in cerebral structures, which is a decisive factor in human evolution. We present the first analysis of manual laterality in a form of object play—stone handling (SH) behavior—in a free-ranging group of Japanese macaques. Defined as a stone-directed manipulative activity, and comprised of multiple one-handed SH patterns (e.g., grabbing a stone in one hand and cradling it against its chest), as well as coordinated two-handed SH patterns with manual role differentiation (e.g., holding a stone with one hand and rubbing it with the other), SH behavior is a good candidate for the study of hand lateralization. We systematically followed the methodological framework developed by McGrew and Marchant (1997) to measure and analyze the presence, strength, and direction of manual preference in the performance of SH behavior and in various SH patterns, both at the individual and group level. Some individuals showed a significant manual lateral bias on a single SH pattern (hand preference), whereas others showed consistency in laterality across all or most of the SH patterns they performed (hand specialization). At the group level, we found that, although their collective distribution of left versus right remained random, most subjects were either significantly but incompletely lateralized, or completely lateralized within particular SH patterns (pattern specialization), but not across all SH patterns (no handedness for SH behavior as a whole). As predicted by the task-complexity model, hand specialization and handedness were stronger in the coordinated bimanual SH patterns than in the unimanual patterns. We discuss the implications of our findings for the evolution of manual preferences in noninstrumental object manipulation versus stone tool use in nonhuman primates and hominins.     

Manual lateralization in early primates: a comparison of two mouse lemur species

In humans, 90% of the population is right handed. Although population hand preference has been found in some primate species, the evolution of manual lateralization in primates is not yet clear. To gain insight into manual lateralization of ancestral primates, we studied hand usage in unspecialized quadrupedal, nocturnal lemurs, using a large sample size. We compared two closely related mouse lemur species to explore the variation of hand preference within the same genus. We tested 44 gray mouse lemurs and 19 Goodman's mouse lemurs in a forced food grasping task. The tests were videotaped. Measures of hand preference (i.e. the hand that is spontaneously chosen for a specific task) and successful hand usage (i.e. the hand that is successful in completing a specific task) were taken to explore manual lateralization. Both species showed manual lateralization at an individual, but not at a population level. Goodman's mouse lemurs showed stronger individual hand preferences than gray mouse lemurs. This suggests that strength in hand preference is variable within the same genus. No sex and age effects were found. The hand preference of offspring was negatively correlated to that of their mothers, but not correlated to that of their fathers. Thus, no clear genetic effect can be derived from these results. In the Goodman's mouse lemurs, hand preference increased with increasing task experience. However, successful hand usage was not affected by task experience, suggesting that successful hand usage is a more stable measurement for manual lateralization than hand preference.     

Baseline cortisol levels and social behavior differ as a function of handedness in marmosets (Callithrix jacchus)

Population hand preferences are rare in nonhuman primates, but individual hand preferences are consistent over a lifetime and considered to reflect an individual's preference to use a particular hemisphere when engaged in a specific task. Previous findings in marmosets have indicated that left‐handed individuals tend to be more fearful than their right‐handed counterparts. Based on these findings, we tested the hypotheses that left‐handed marmosets are (a) more reactive to a social stressor and (b) are slower than right‐handed marmosets in acquiring a reversal learning task. We examined the hand preference of 27 male and female marmosets (ages of 4–7 years old) previously tested in a social separation task and a reversal learning task. Hand preference was determined via a simple reaching task. In the social separation task, monkeys were separated from their partner and the colony for a single 7‐hr session. Urinary cortisol levels and behavior were assessed at baseline, during the separation and 24 hr postseparation. Hand preferences were equally distributed between left (n = 10), right‐handed (n = 10), and ambidextrous (n = 7) individuals. The separation phase was associated with an increase in cortisol levels and behavioral changes that were similar across handedness groups. However, cortisol levels at baseline were positively correlated with right‐handedness, and this relationship was stronger in females than in males. In addition, the occurrence of social behaviors (pre‐ and postseparation) was positively correlated with right‐handedness in both sexes. Baseline cortisol levels did not correlate significantly with social behavior. Acquisition of the reversals was poorer in females than males but did not differ as a function of handedness. We conclude that (a) both stress reactivity and cognitive flexibility are similar across handedness groups and (b) left‐handers exhibit less social behavior and have lower basal cortisol levels than ambidextrous and right‐handed subjects. The underlying causes for these differences remain to be established.     

Hand preferences on unimanual and bimanual tasks in Tonkean macaques (Macaca tonkeana)

This is the first study to examine hand preferences in Tonkean macaques on a bimanual task. One of our objectives was to continue the move toward greater task standardization, in order to facilitate comparisons between species and studies on handedness. The main aim was to test and determine task robustness, by varying intra‐task complexity. To this end, we administered several different tasks to the subjects: two unimanual tasks (grasping task featuring items of different sizes) and three coordinated bimanual tasks (tube task involving different materials, weights, and diameters). Although we found no significant hand preference in either task at the group level, the macaques were more strongly lateralized for small items than for large ones in the unimanual grasping task. Moreover, the absence of a correlation between these two versions of the unimanual task confirmed the weakness of this grasping task for assessing handedness. Regarding the bimanual tube task, no difference was found between the three versions in either the direction or the strength of hand preference. Moreover, the highly correlated hand preferences between these three versions suggest that the tube task provides a more robust means of measuring manual preferences. Am J Phys Anthropol 152:315–321, 2013. © 2013 Wiley Periodicals, Inc.     

Laterality in spontaneous motor activity of chimpanzees and squirrel monkeys

Varieties of nonmanipulative motor responses were observed in chimpanzees and squirrel monkeys. Chimpanzees displayed a right hand preference for touching their inanimate environments but used their right and left hands equally for touching their faces and their bodies. The latter result was not consistent with previous reports of a left hand preference for face touching in apes. The right hand preference for environmental touching was stronger in male than in female chimpanzees. Squirrel monkeys had a right preference for combined hand and foot responses directed to their bodies, but expressed no handedness for environmentally directed touching. These limb preferences in chimpanzees and squirrel monkeys indicate that neither precise, complex manipulation nor postural instability are necessary conditions for population level hand preferences. Factor analysis of the chimpanzee manual responses showed distinct self and environmentally directed factors. Analysis of the squirrel monkey data also showed self and environmental factors, except that body scratching had a negative loading on the environmental factor. This latter result suggests that self-scratching by squirrel monkeys is a displacement activity that suppresses manual exploration of the environment. © 1992 Wiley-Liss, Inc.     

Limb use and preferences in wild orang-utans during feeding and locomotor behavior

Limited data are available on hemispheric lateralization in wild orang-utans. There has been only one previous investigation of limb preferences in wild orang-utans [Yeager, 1991]. We examined the lateralization of limb use in wild Bornean orang-utans (Pongo pygmaeus pygmaeus) with the aim of providing more insight into possible hemispheric specialization in wild nonhuman primates. Here, we report in detail on limb use and preference during arboreal locomotion between trees (N=6) and on feeding involving one limb (N=8) and two limbs (N=6). We distinguished between locomotion between overlapping trees (Type I) and locomotion involving gap crossing (Types II and III). For locomotion Type I, the six orang-utans showed no leading hand preference, however for locomotion Types II and III, all six showed significant right-hand preferences. All eight orang-utans showed individual hand preferences for reaching for food, but no significant group bias was found. Limb preferences for feeding involving two limbs (hand-hand or hand-foot) differed between juveniles (right hand-right foot), adult females (left hand-right hand) and adult males (right hand-left hand). Although not present for all tasks, the results indicate that orang-utans do show evidence of hemispheric specialization, but the use of the hands is not under a strong lateralized hemispheric control and is adaptable.     

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.     

Hand Preferences for Bimanual Coordination in 77 Bonobos (<Emphasis Type="Italic">Pan paniscus</Emphasis>): Replication and Extension

The literature on manual laterality in nonhuman primates provides inconsistent and inconclusive findings and is plagued by methodological issues (e.g., small samples, inconsistency in methods, inappropriate measures) and gaps. Few data are available on bonobos and these are only from small samples and for relatively simple tasks. We examined laterality in a large sample of bonobos for a complex task. We tested 48 bonobos from Lola Ya Bonobo sanctuary (DR Congo) in an extension of our previous study of 29 bonobos from 3 European zoos. We assessed hand preferences using the tube task, which involves bimanual coordination: one hand extracts food from a tube that is held by the other hand. This task is a good measure of laterality and it has been used in other studies. We recorded events (frequency) and independent bouts of food extraction. We found significant manual laterality, which was not influenced by the settings or rearing history. We observed little effect of sex and found an influence of age, with greater right hand use in adults. The laterality was marked, with strong preferences and most individuals being lateralized (when analyzing frequency). We found individual preferences, with no group-level bias, even when we combined the data from the sanctuary and the zoos to enlarge the sample to 77. These first data, for a complex task and based on a large sample, are consistent with previous findings in bonobos and in other nonhuman primate species for a variety of tasks. They suggest that, despite particular features in terms of proximity to humans, language and bipedalism, bonobos do not display a laterality that is more marked or more similar to human handedness compared to that of other nonhuman primate species.     

Hand preference in the Sifaka (propithecus verreauxi coquereli) during feeding in captivity

The Coquerel's sifakas were chosen for this study on hand preference because little is known about handedness in Indriidae. Fifteen Coquerel's sifakas were observed at the Duke University Primate Center as they fed on chopped fruit, vegetables, and primate chow. Analysis of age, sex, and hand preference indicated that the adult males both individually and as a group tended toward left-handedness. Adult females as a group did not show a trend in the direction of handedness. However, individual adult females showed consistent right- or left-hand preference. Younger sifakas tended toward ambipreference, suggesting that lateralization of hand preference is gradual, becoming more stable in adulthood. These findings suggest that sex and age may be strong indicators for lateralization of hand preference in Coquerel's sifakas. Duke University Primate Research Center Publication 292     

Laterality in quadrupedal and bipedal prosimians: Reach and whole-body turn in the mouse lemur (Microcebus murinus) and the galago (Galago moholi)

Lateral preferences in food reaching and whole-body turning were assessed in 24 prosimian primates: 16 galagos (Galago moholi) and 8 mouse lemurs (Microcebus murinus). Reach and turn preference in the galago were examined using a single testing procedure; separate procedures were used to evaluate reach and turn preferences in the mouse lemur. The motoric requirements for both species were 1) reach into a Plexiglas container with a single hand for a food item and 2) execution of a whole-body rotation about the long axis of the body. Twenty-three of the subjects tested had a reach preference (15 right, 8 left preferent) and 22 a turn preference (1 right and 21 left preferent). No correlation between the direction of reach and turn preference was found for either species; however an association between right reach preference and female gender was found for the galagos. A species difference in the strength of lateralization was found, with the more bipedal species, the galago, more strongly lateralized in both measures. This result supports the hypothesis that the assumption of upright posture was an important factor in the phylogenetic development of primate lateralization.     

Brief communication: Captive gorillas are right‐handed for bimanual feeding

Predominance of right‐handedness has historically been considered as a hallmark of human evolution. Whether nonhuman primates exhibit population‐level manual bias remains a controversial topic. Here, we investigated the hypothesis that bimanual coordinated activities may be a key‐behavior in our ancestors for the emergence and evolution of human population‐level right‐handedness. To this end, we collected data on hand preferences in 35 captive gorillas (Gorilla gorilla) during simple unimanual reaching and for bimanual coordinated feeding. Unimanual reaching consisted of grasping food on the ground, while bimanual feeding consisted of using one hand for holding a food and processing the food item by the opposite hand. No population‐level manual bias was found for unimanual actions but, in contrast, gorillas exhibited a significant population‐level right‐handedness for the bimanual actions. Moreover, the degree of right‐handedness for bimanual feeding exceeds any other known reports of hand use in primates, suggesting that lateralization for bimanual feeding is robust in captive gorillas. The collective evidence is discussed in the context of potential continuity of handedness between human and nonhuman primates. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.