Handedness In Nonhuman Primates Research Articles

Insights Into Human and Nonhuman Primate Handedness From Measuring Both Hands

Handedness is part of our everyday lives, but where does it come from? Researchers studying nonhuman primates and young children have approached this question from different perspectives—evolutionary and developmental, respectively. Their work converges on the conclusion that measurement matters in the science of handedness. Coming to a consensus on assessment will guide future research into the origins of handedness. A candidate behavior for promoting multidisciplinary comparison is role-differentiated bimanual manipulation.

Hand preference on unimanual and bimanual tasks in Barbary macaques (Macaca sylvanus)

The presence of group-level handedness in non-human primates remains controversial, as different studies have produced inconsistent results. Bimanual coordinated tasks have been found to elicit more pronounced hand preferences than simple unimanual tasks. The aim of this study was to examine manual lateralization in a group of 15 Barbary macaques during unimanual and bimanual tasks. In the unimanual task, data on simple food reaching in a foraging context were collected. During the bimanual task, macaques had to use one hand to hold a tube-shaped apparatus while reaching with the other hand to retrieve the food inside it. Data on the hand use to retrieve food were collected. First, no significant group-level hand preference was found for the unimanual task. However, a significant right hand bias was evident for the bimanual task. At the individual-level, approximately 47% and 67% of the subjects had a significant hand preference in the unimanual and bimanual task respectively. The strength of the hand preference was greater in the bimanual than in the unimanual task. Findings of this study add Macaca sylvanus to the other species showing a right hand preference for coordinated bimanual tasks. Moreover, our results add to the growing body of evidence that bimanual tasks are more suitable and valid measures to investigate handedness in non-human primates.

Division of Labour:A Democratic Approach towards Understanding Manual Asymmetries in Non-Human Primates

A consequence of the 'gold rush'-like hunch for human-like handedness in non-human primates has been that researchers have been continually analysing observations at the level of the population, ignoring the analysis at the level of an individual and, consequently, have potentially missed revelations on the forms and functions of manual asymmetries. Recently, consecutive studies on manual asymmetries in bonnet macaques, Macaca radiata revealed both the functional and adaptive significance of manual asymmetries respectively, and pointed towards the division of labour as being the general principle underlying the observed hand-usage patterns. We review the studies on manual asymmetries in capuchin monkeys, Cebus spp. and argue that the observed hand-usage patterns might reflect specialization of the two hands for accomplishing tasks that require different dexterity types (i.e. manoeuvring in three-dimensional space or physical strength). To this end, we do a step-by-step analysis of the various tasks used in the studies on manual asymmetries in capuchin monkeys. We then describe the division of labour as a general principle underlying manual asymmetries in non-human primates and propose experimental designs that would elaborate the forms and functions of manual asymmetries in non-human primates and the associated adaptive value.

Handedness for Unimanual Grasping in 564 Great Apes: The Effect on Grip Morphology and a Comparison with Hand Use for a Bimanual Coordinated Task.

A number of factors have been proposed to influence within and between species variation in handedness in non-human primates. In the initial study, we assessed the influence of grip morphology on hand use for simple reaching in a sample of 564 great apes including 49 orangutans Pongo pygmaeus, 66 gorillas Gorilla gorilla, 354 chimpanzees Pan troglodytes and 95 bonobos Pan paniscus. Overall, we found a significant right hand bias for reaching. We also found a significant effect of the grip morphology of hand use. Grasping with the thumb and index finger was more prevalent in the right compared to left hand in all four species. There was no significant sex effect on the patterns of handedness. In a subsample of apes, we also compared consistency in hand use for simple reaching with previously published data on a task that measures handedness for bimanual actions. We found that the ratio of subjects with consistent right compared to left hand use was more prevalent in bonobos, chimpanzees and gorillas but not orangutans. However, for all species, the proportion of subjects with inconsistent hand preferences between the tasks was relatively high suggesting some measures may be more sensitive in assessing handedness than others.

Evaluating handedness measures in spider monkeys.

Despite long-standing interest and a vast body of literature, there is still disagreement as to how handedness should be measured in nonhuman primates. The primary goal of this study was to evaluate two common measures of handedness in nonhuman primates using the spider monkey, a unique study species due to its lack of a thumb and limited dexterity. Contrary to our predictions and previous findings in Ateles, there was no evidence for group-level hand biases on either the coordinated bimanual TUBE task or a unimanual reaching task. At the individual level, monkeys exhibited preferences on both tasks. There was a leftward trend on the bimanual task and a rightward trend on the unimanual task. Monkeys that were strongly lateralized on the bimanual task showed a comparable hand preference on the unimanual task, whereas monkeys with a moderate preference on the bimanual task shifted to the opposite hand on the unimanual task. Comparing across measures, the two hand-use patterns reported (consistent and shift) might have obscured group-level findings, given the available sample size. Overall, these data reaffirm that task type influences hand use in primates, and multiple measures are needed to fully characterize the construct of handedness. Consideration should be given to the difficulty required between tasks as well as between species.

Division of labor in hand usage in free‐ranging bonnet macaques, Macaca radiata

Primates exhibit laterality in hand usage either in terms of (a) hand with which an individual solves a task or while solving a task that requires both hands, executes the most complex action, that is, "hand preference," or (b) hand with which an individual executes actions most efficiently, that is, "hand performance." Observations from previous studies indicate that laterality in hand usage might reflect specialization of the two hands for accomplishing tasks that require maneuvering dexterity or physical strength. However, no existing study has investigated handedness with regard to this possibility. In this study, we examined laterality in hand usage in urban free-ranging bonnet macaques, Macaca radiata with regard to the above possibility. While solving four distinct food extraction tasks which varied in the number of steps involved in the food extraction process and the dexterity required in executing the individual steps, the macaques consistently used one hand for extracting food (i.e., task requiring maneuvering dexterity)-the "maneuvering" hand, and the other hand for supporting the body (i.e., task requiring physical strength)-the "supporting" hand. Analogously, the macaques used the maneuvering hand for the spontaneous routine activities that involved maneuvering in three-dimensional space, such as grooming, and hitting an opponent during an agonistic interaction, and the supporting hand for those that required physical strength, such as pulling the body up while climbing. Moreover, while solving a task that ergonomically forced the usage of a particular hand, the macaques extracted food faster with the maneuvering hand as compared to the supporting hand, demonstrating the higher maneuvering dexterity of the maneuvering hand. As opposed to the conventional ideas of handedness in non-human primates, these observations demonstrate division of labor between the two hands marked by their consistent usage across spontaneous and experimental tasks requiring maneuvering in three-dimensional space or those requiring physical strength.

Comparing human and nonhuman primate handedness: challenges and a modest proposal for consensus.

In the past 20-25 years, there have been a number of studies published on handedness in nonhuman primates. The goal of these studies has been to evaluate whether monkeys and apes show patterns of hand preference that resemble the right-handedness found in the human species. The extant findings on handedness in nonhuman primates have revealed inconsistent evidence for population-level handedness within and between species. In this article, I discuss some of the methodological and statistical challenges to comparative studies of handedness in human and nonhuman primates. I further offer a framework for developing some consensus on evaluating the validity of different handedness measures and the characterization of individual hand preferences.

Independence of data points in the measurement of hand preferences in primates: Statistical problem or urban myth?

Lack of independence of data points or the pooling fallacy has been suggested as a potential problem in the study of handedness in nonhuman primates, particularly as it relates to whether hand use responses should be recorded as individual events or bouts of activity. Here, I argue that there is no evidence that the concept of statistical independence of data points or the pooling fallacy is a problem in the evaluation of population-level handedness in previous studies in nonhuman primates. I further argue these statistical concepts have been misapplied to the characterization of individual hand preferences. Finally, I argue that recording hand use responses as bouts rather than events has no significant effect on reports of hand use in nonhuman primates and, in fact, may unintentionally bias hand use toward the null hypothesis. Several suggestions for improvement in the measurement and statistical determination of individual handedness are offered in the article.

Within- and between-task consistency in hand use as a means of characterizing hand preferences in captive chimpanzees (Pan troglodytes).

There remain considerable questions regarding the evidence for population-level handedness in nonhuman primates when compared with humans. One challenge in comparing human and nonhuman primate handedness involves the procedures used to characterize individual handedness. Studies of human handedness use consistency in hand use within and between tasks as a basis for hand preference classification. In contrast, studies of handedness in nonhuman primates use statistical criteria for classifying handedness. In this study, we examined within- and between-task consistency in hand use as a means of characterizing individual handedness in a sample of 300 captive chimpanzees (Pan troglodytes). Chimpanzees showed population-level right-handedness for both within- and between-tasks consistency, though the proportion of right-handed chimpanzees was lower than what has typically been reported for humans. We further found that there were small, but significant, associations in hand use between measures. There were no significant sex or colony effects on the distribution of handedness. The results are discussed in the context of theories on the evolution of handedness in nonhuman primates.

Sex difference in squirrel monkeys’ handedness for unimanual and bimanual coordinated tasks

Whether nonhuman primates exhibit population-level manual bias remains controversial. There is a growing body of evidence showing consistent individual lateralization and population-level handedness particularly for complex manual behaviours such as bimanual coordinated actions in both monkeys and apes. Whereas the few published studies on hand preferences in squirrel monkeys, Saimiri sciureus, have focused only on unimanual behaviours and generally failed to elicit population-level handedness, we report in this paper the first set of data on hand use for a bimanual coordinated behaviour elicited by the manipulation of an artificial tube in a sample of 37 captive-born squirrel monkeys. The task consisted of holding an opaque tube with one hand and removing the food inside the tube with the other hand. For comparison, hand use data were collected from 38 subjects for unimanual reaching for food from an experimenter when the squirrel monkeys were clinging vertically on the door of the cage. For bimanual coordinated actions, we found a nonsignificant trend towards left-handedness at a population level, especially in males, whereas unimanual reaching when clinging elicited a significant predominance of right-handedness, especially in females. These results are discussed within comparative approaches across primate species and within different theoretical frameworks about the determining factors of handedness in nonhuman primates.

Hand preferences for coordinated bimanual actions in 777 great apes: Implications for the evolution of handedness in Hominins

Whether or not nonhuman primates exhibit population-level handedness remains a topic of considerable scientific debate. Here, we examined handedness for coordinated bimanual actions in a sample of 777 great apes including chimpanzees, bonobos, gorillas, and orangutans. We found population-level right-handedness in chimpanzees, bonobos and gorillas, but left-handedness in orangutans. Directional biases in handedness were consistent across independent samples of apes within each genus. We suggest that, contrary to previous claims, population-level handedness is evident in great apes but differs among species as a result of ecological adaptations associated with posture and locomotion. We further suggest that historical views of nonhuman primate handedness have been too anthropocentric, and we advocate for a larger evolutionary framework for the consideration of handedness and other aspects of hemispheric specialization among primates.

Effects of early adverse experiences on behavioural lateralisation in rhesus monkeys (Macaca mulatta)

In the past 15 to 20 years, evidence of population-level handedness in non-human primates has emerged from a plethora of studies, although considerable inconsistency is also apparent. The study reported here examined two factors that may contribute to the expression of hand preference: early rearing history and sex differences. Handedness was assessed in rhesus monkeys (Macaca mulatta) using a task that measures coordinated bimanual actions and is referred to as the TUBE task. Nursery-reared monkeys demonstrated greater left-hand bias in the TUBE task when compared to their mother-reared counterparts. Females showed greater right-hand preference and stronger bias on the TUBE task compared to males. These results provide evidence that early rearing experiences significantly influence the development of lateralisation in nonhuman primates.

Parental and perinatal factors influencing the development of handedness in captive chimpanzees

It has been proposed that human right handedness is determined by genetic factors associated with the emergence of language, whereas non-human primate handedness is determined by random, non-genetic factors. These different mechanisms account for differences in the distribution of handedness between human and non-human primates. Here we report evidence that genetic factors play a role in the determination of handedness in chimpanzees. We further report that differential rearing has no influence on the expression of handedness in related individuals. Contrary to many theories of the origin of handedness, these results indicate that genetic factors have a significant influence on handedness in chimpanzees.

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.

Chimpanzee (Pan troglodytes) handedness: variability across multiple measures of hand use.

This study examined intertask consistency in handedness across multiple measures of hand use in a sample of 187 chimpanzees (Pan troglodytes). Hand preferences for 2 to 6 measures were collected from the sample, and hand preference scores were derived on the basis of the individual hand preferences for each measure. Seven of 15 possible intratask correlations were significant, with some degree of clustering depending on the motor demands of the tasks. Two overall measures of handedness revealed population-level right-handedness in the chimpanzees, although the degree of bias was reduced for chimpanzees tested on more than 3 measures of hand use. The results are interpreted in the context of several recent studies that proposed theoretical models of handedness in nonhuman primates.

On the other hand : Statistical issues in the assessment and interpretation of hand preference data in nonhuman primates

I describe methodological and statistical issues in the assessment of hand preference in nonhuman primates and discuss them in the context of a recent paper by McGrew and Marchant (1997) in which they conclude that there is no convincing evidence of population-level hand preferences in nonhuman primates. The criteria used by them to evaluate individual and population-level hand preferences are flawed, which results in an oversimplification of findings in nonhuman primates. I further argue that the classification schema used by McGrew and Marchant (1997) to compare hand preference distributions between species is theoretically weak and does not offer a meaningful way to compare human and nonhuman primate handedness.

Chimpanzee handedness revisited: 55 years since Finch (1941)

Chimpanzees and other great apes have long held the fascination of psychologists because of their morphological and behavioral similarities to humans. This paper describes the historical interest in studies on chimpanzee handedness and reviews current findings. Data are presented which suggest that transient changes in posture result in the transient expression of right-handedness in chimpanzees. The role of tool use as an evolutionary mechanism underlying the expression of right-handedness is challenged. Rather, emphasis is placed on the role of bimanual feeding as a behavioral adaptation for the expression of handedness. Suggestions for further research on the nature of nonhuman primate handedness are made in light of these findings.

A 'Handy' Guide to Primate Evolution

A 'Handy' Guide to Primate Evolution

Note on hand use in the manipulation of joysticks by rhesus monkeys (Macaca mulatta) and chimpanzees (Pan troglodytes).

In a recent article MacNeilage, Studdert-Kennedy, and Lindblom (1987) proposed that nonhuman primate handedness may be contingent on the specific task requirements with visual-spatial tasks yielding left-hand preferences and fine motor tasks producing right-hand preferences. This study reports hand preferences in the manipulation of joysticks by 2 rhesus monkeys (Macaca mulatta) and 3 chimpanzees (Pan troglodytes). Reach data were also collected on these same subjects and served as a basis for comparison with preference data for manipulation of the joystick. The data indicated that all 5 subjects demonstrated significant right-hand preferences in manipulating the joystick. In contrast, no significant hand preferences were found for the reach data. Reaction time data also indicated that the right hand could perform a perceptual-motor task better than the left hand in all 5 subjects. Overall, the data indicate that reach tasks may not be sensitive enough measures to produce reliable hand preferences, whereas tasks that assess fine motor control produce significant hand preferences.

Hand preference for visually guided reaching in human infants and adults

As the collection of new research reports in this volume shows, the question of handedness in non-human primates has become a subject of intense interest among psychologists and primatologists. The historical evidence also shows that this interest is of long standing (see Harris, Ch. 1, this volume). Still, the question remains controversial. There is a measure of agreement that individual animals show reliable hand preference but no consensus that this is a species characteristic.