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.     

Patterns of lateralized hand use in an arboreal primate, Simias concolor

Studies of hand use in nonhuman primates suggest that several species exhibit hand preferences for a variety of tasks. The majority of studies, however, focus on the lateralized hand use of captive nonhuman primate populations. Although captive settings offer a more controlled environment for assessing hand preferences, studies of wild populations provide important insights into how handedness is affected by natural environmental conditions and thus potential insights into the evolution of handedness. To investigate handedness in a population of wild nonhuman primates, we studied patterns of lateralized hand use during feeding in four simakobu monkeys (Simias concolor), an arboreal species inhabiting the Mentawai Islands, Indonesia. Our data show that individual variation in hand preferences for feeding existed among our study animals. In addition, each simakobu expressed a significant hand preference for supporting itself on a branch during feeding, an uncoordinated bimanual task. This bias was most prevalent when the branch used for support was a main branch rather than a terminal branch. When both hands were employed in a coordinated bimanual feeding activity (bimanual manipulation), only two subjects showed a significant bias for feeding. Our data suggest that these individuals are more likely to express significant hand preferences when feeding from stable, rather than precarious, positions within the canopy.     

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.     

Chimpanzee right-handedness reconsidered: Evaluating the evidence with funnel plots

Evidence for population-level right-handedness in nonhuman primates seems inconsistent and contradictory, and many hypotheses have been advanced to account for this volatility. Funnel plots (scatter plots of percent right-hand use vs. sample size) offer a straightforward graphical technique for assessing: 1) the strength and consistency of handedness, 2) whether variability is consistent with normal sampling variation, and 3) how likely reports of statistically significant handedness might have arisen due to chance (i.e., type I error). They are informative for both within- and among-population variation. Reexamination of within-population variation from a detailed and widely cited study reporting significant population-level right-handedness in 140 individual captive chimpanzees (Hopkins [1994] Dev. Psychobiol. 27:395-407) revealed several puzzling patterns: 1) funnel plots showed higher percent right-hand use among individuals for which fewer observations were recorded, 2) when individuals with fewer than 25 observations were excluded, statistical support for population-level right-handedness either became marginal (P = 0.043, when computed as average percent use of the right hand) or disappeared (P = 0.62, when computed as proportion of individuals using the right hand more than the left, whether they did so significantly or not), and 3) the proportion of statistically ambilateral chimpanzees actually increased with increasing number of observations per individual, rather than decreased as would be expected for true population-level right-handedness. In addition, funnel plots of among-population variation from an earlier meta-analysis (McGrew and Marchant [1997] Yrbk. Phys. Anthropol. 40:201-232) suggested that the four reports of significant right-handedness, out of 37 estimates from 14 studies, were likely those that achieved statistical significance simply due to chance. Funnel plots, and the more refined statistical tests they suggest, confirm that the current evidence for population-level right-handedness in chimpanzees remains equivocal.     

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.     

Anthropomorphism,primatomorphism, mammalomorphism: understanding cross-species comparisons

The charge that anthropomorphizing nonhuman animals is a fallacy is itself largely misguided and mythic. Anthropomorphism in the study of animal behavior is placed in its original, theological context. Having set the historical stage, I then discuss its relationship to a number of other, related issues: the role of anecdotal evidence, the taxonomy of related anthropomorphic claims, its relationship to the attribution of psychological states in general, and the nature of the charge of anthropomorphism as a categorical claim. I then argue that the categorical reading of anthropomorphism cannot work and that it misrepresents what is being claimed when one claims that traits are shared between humans and nonhumans. We should think of such claims not as anthropomorphic per se– because that implies the trait is intrinsically human and only derivatively nonhuman. Instead, traits shared with mammals are mammalomorphic, for example, or primatomorphic when shared by primates.     

Termite fishing laterality in the fongoli savanna chimpanzees (Pan troglodytes verus): Further evidence of a left hand preference

Whether nonhuman primates show population‐level handedness is a topic of much scientific debate. A previous study of handedness for termite fishing reported population‐level left handedness in the chimpanzees from Gombe National Park, Tanzania. In the current study, we examined whether similar hand preferences were evident in a savanna‐dwelling chimpanzee population with regards to termite fishing. Hand preference data were collected for 27 chimpanzees from February 2007 through July 2008 and November 2011 through January 2012 in southeastern Senegal. Overall, the Fongoli chimpanzees demonstrate a trend toward population‐level handedness, though the results did not reach conventional levels of statistical significance likely due to the limited sample size. Fongoli chimpanzees showed the same pattern of left hand preference as reported at Gombe and the two populations did not differ significantly. When the data were combined across all studies, wild chimpanzees showed a population‐level left hand preference for termite fishing. Am J Phys Anthropol, 2012. © 2012 Wiley Periodicals, Inc.     

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.     

Handedness and Grooming in Pan troglodytes: Comparative Analysis Between Findings in Captive and Wild Individuals

Grooming is a complex set of motor actions, common in highly social primates. We tested for asymmetries in hand use during unimanual and bimanual allogrooming in 215 captive chimpanzees. In addition to hand use, we coded in the ethogram whether the manual grooming action co-occurred with the use of the mouth. Overall, grooming did not elicit strong handedness at the individual level, but there is a small yet significant population-level right-hand bias for bimanual grooming. Mouth use during grooming had no influence on hand use. A comparison of the findings with previously published data on handedness for grooming in wild chimpanzees suggests that wild apes are more right-handed than captive individuals are for allogrooming. Collectively, the results suggest that role differentiation of the hands is an important factor in the assessment of handedness for grooming, and perhaps additional manual actions of chimpanzees and other primates.     

Lateral bias to the leading limb in an olfactory social signal by male ring-tailed lemurs

Because ring-tailed lemurs (Lemur catta) show handedness during feeding, I investigated whether they also show lateral preference in the limbs used by males during scent marking. During a bout of marking, a male alternates a variable number of shoulder rubs and arm marks. It is a complex social signal that has both olfactory and visual components and is frequently part of intrasexual agonistic interactions. I used all-occurrences behavior sampling, manually recorded all totally visible bouts, and required a minimum of 50 bouts per animal. The subjects included six wild and four group-living captive male lemurs. I considered limb usage to be lateralized for each individual lemur if the frequency of use of one side was significantly above chance as determined by binomial z-scores at P<.05. I measured consistency of lateral preference by calculating handedness index (HI) scores for each individual. Overall, I recorded 1,583 bouts of scent marking, and 66% of the bouts began with shoulder rubbing. Eight of the 10 males showed a significant, moderately strong lateral preference for the lead limb in the first shoulder rub performed in a bout, and for six of these eight the preferred lead limb for shoulder rubbing was the left one. Six of the 10 males showed a significant but weak lateral preference in the first arm mark, and five of these preferred the opposite limb to that used for the first shoulder rub. Although the preferences were not at the population level, eight of the 10 lemurs showed a lateral bias in the lead limb used for a component of this complex social signal.     

Brief communication: Hand preference for bimanual and unimanual feeding in captive gorillas: extension in a second colony of apes

Right-hand dominance is widely considered to be a uniquely human trait. Whether nonhuman primates exhibit similar population-level hand preferences remains a topic of considerable debate. Despite extensive research focusing on laterality in nonhuman primates, our interpretation of these studies is limited due to methodological issues including the lack of a common measure of hand preference and the use of tasks that may not be reliable indicators of handedness. The use of consistent methods between studies is necessary to enable comparisons within and between species and allow for more general conclusions to be drawn from these results. The present study replicates methods used in recent research reporting population-level right-handedness in captive gorillas (Meguerditchian et al.,2010). Observational data were collected on hand preference for unimanual and bimanual feeding in 14 captive western lowland gorillas (Gorilla gorilla gorilla). Individual-level preferences were found, primarily for bimanual feeding; however, the data reveal no group-level directional bias (contra Meguerditchian et al.). Like the study by Meguerditchian et al. (2010), though, bimanual feeding revealed significantly stronger hand preferences than unimanual reaching, and age, sex, group membership, or rearing history had no effect on hand preference. Finally, variations in diet and corresponding grip type between studies suggest that hand preferences may vary across bimanual tasks depending on grip morphology. This study aims to contribute to our existing knowledge of primate laterality by increasing the number of individuals investigated using methods that allow for comparisons with similar research.     

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.     

Technical note: Quantification of neurocranial shape variation using the shortest paths connecting pairs of anatomical landmarks

Three‐dimensional geometric morphometric techniques have been widely used in quantitative comparisons of craniofacial morphology in humans and nonhuman primates. However, few anatomical landmarks can actually be defined on the neurocranium. In this study, an alternative method is proposed for defining semi‐landmarks on neurocranial surfaces for use in detailed analysis of cranial shape. Specifically, midsagittal, nuchal, and temporal lines were approximated using Bezier curves and equally spaced points along each of the curves were defined as semi‐landmarks. The shortest paths connecting pairs of anatomical landmarks as well as semi‐landmarks were then calculated in order to represent the surface morphology between landmarks using equally spaced points along the paths. To evaluate the efficacy of this method, the previously outlined technique was used in morphological analysis of sexual dimorphism in modern Japanese crania. The study sample comprised 22 specimens that were used to generate 110 anatomical semi‐landmarks, which were used in geometric morphometric analysis. Although variations due to sexual dimorphism in human crania are very small, differences could be identified using the proposed landmark placement, which demonstrated the efficacy of the proposed method. Am J Phys Anthropol 151:658–666, 2013. © 2013 Wiley Periodicals, Inc.     

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 Preference in Free-Ranging White-Throated Capuchins (Cebus capucinus) in Costa Rica

I studied the hand preference patterns of individuals in three troops of white-throated capuchins (C. capucinus) in Palo Verde, Costa Rica, during 11 months from February 1995 to January 1996. I used focal and ad libitum sampling techniques and tested several frameworks that seek to explain and to predict primate hand use patterns via a variety of spontaneous tasks that differ in manipulative difficulty and required postural regulation: reach, tap, grab, carry, and object-use. The monkeys showed symmetrical hand use patterns for the easy tasks, reach and tap; strongly asymmetrical patterns for the highly manipulative task, object-use, at the individual level; and weak population-level biases for tasks requiring a degree of postural regulation, carry. The results for data on grab are inconclusive. These results do not support the available primate hand use frameworks and differ from most of the captive literature on hand preference in Cebus. The findings indicate that postural regulation may influence hand use patterns in nonhuman primates at the population level.     

Ecological modelling in an evolutionary context

I argue that one of the strong features in disciplines like molecular biology and cosmology is the extent ot which they use a powerful theoretical framework to generate and test quantitative predictions. Studies of biological evolution can exploit a similar advantage by integrating our current understanding of physiological and sociobiological processes to generate models of much greater sophistication than has commonly been the practice hitherto. I illustrate this with a number of examples drawn from the evolutionary biology of human and nonhuman primates.     

Handedness in wild chimpanzees

The debate over nonhuman primate precursors to human handedness is unsettled mainly due to lack of data, particularly on apes. Handedness in wild chimpanzees at the Taï National Park Côte d'Ivoire, has been monitored in four tasks. For the simple unimanual ones, reaching and grooming, adults use both hands equally (ambidextrous), while for the more complex unimanual wadge-dipping and the complex bimanual nut-cracking, adults are highly lateralized. These results support the hypothesis that lateralization increases with the complexity of the task. The lateralization is constant for years for each task but may vary in an individual with respect to different tasks. For nutcracking females are more lateralized than males. The ontogeny of handedness for nut-cracking shows many variations in the tendency to use one hand and in the side preferred, until at about 10 years of age, the individual achieves her adult handedness. No population bias toward one side exists in Taï chimpanzees. No heritability of handedness between mother and offspring was observed. Human and chimpanzees handedness are compared.     

Models of focal cerebral ischemia in the nonhuman primate

Ischemic stroke is a uniquely human disease syndrome. Models of focal cerebral ischemia developed in nonhuman primates provide clinically relevant platforms for investigating pathophysiological alterations associated with ischemic brain injury, microvascular responses, treatment responses, and clinically relevant outcomes that may be appropriate for ischemic stroke patients. A considerable number of advantages attend the use of nonhuman primate models in cerebral vascular research. Appropriate development of such models requires neurosurgical expertise to produce single or multiple vascular occlusions. A number of experimentally and clinically accessible outcomes can be measured, including neurological deficits, neuron injury, evidence of non-neuronal cell injury, infarction volume, real-time imaging of injury development, vascular responses, regional cerebral blood flow, microvascular events, the relation between neuron and vascular events, and behavioral outcomes. Nonhuman primate models of focal cerebral ischemia provide excellent opportunities for understanding the vascular and cellular pathophysiology of cerebral ischemic injury, which resembles human ischemic stroke, and the appropriate study of pharmacological interventions in a human relevant setting.     

Guidelines for developing and managing an environmental enrichment program for nonhuman primates.

Before implementing an environmental enrichment program for nonhuman primates, several issues should be considered. The assignment of enrichment tasks can be made to caretakers, a dedicated "enrichment technician," volunteers, students or individuals with training in behavioral science. Determining the enrichment techniques to be used must take into account personnel time available; the species, age, sex, and individual histories of the nonhuman primates; and experimental protocols for which animals are being maintained. Identifying the most beneficial way to use the available personnel time must be tailored for each institution. To meet federal regulations, records must be kept of the environmental enhancements available to each nonhuman primate. Good record-keeping will allow appropriate evaluation of the program. This evaluation should involve the animals' responses to the enrichment opportunity, cost and durability of enrichment items, human and nonhuman safety considerations, and personnel required. The well-being of captive nonhuman primates will be most improved if well-informed decisions are made in developing and managing environmental enrichment programs.     

Handedness in great apes: A review of findings

We present data on hand preference in great apes and discuss them in the context of theoretical models of hand preference in nonhuman primates presented by MacNeilageet al. (1987) and by Fagot and Vauclair (1991). We also discuss several methodological and statistical issues as they pertain to the assessment of hand preference in great apes and other primate species. Finally, we present a comparative framework for the study of hand preference, emphasizing the importance of studies with great apes in developing evolutionary models of hemispheric specialization.