Does body posture influence hand preference in an ancestral primate model?

Background  

The origin of human handedness and its evolution in primates is presently under debate. Current hypotheses suggest that body posture (postural origin hypothesis and bipedalism hypothesis) have an important impact on the evolution of handedness in primates. To gain insight into the origin of manual lateralization in primates, we studied gray mouse lemurs, suggested to represent the most ancestral primate condition. First, we investigated hand preference in a simple food grasping task to explore the importance of hand usage in a natural foraging situation. Second, we explored the influence of body posture by applying a forced food grasping task with varying postural demands (sit, biped, cling, triped).     

Hand preference in unimanual and bimanual tasks and postural effect on manual laterality in captive red-capped mangabeys (Cercocebus torquatus torquatus)

Hand preference in 11 captive red-capped mangabeys (Cercocebus torquatus torquatus) was examined under different conditions: a free situation during spontaneous food processing, three different postural conditions (brachiating, and bipedal and tripedal standing), and a situation involving bimanual processing. Generally, individual laterality was found regardless of the task and behavior involved. However, the number of monkeys with hand preferences and the strength of the preference increased with the complexity of the tasks. The monkeys exhibited a significantly higher and positive mean manual preference index (HI) when they were hanging than when they were quadrupedal or sitting. The strength of manual preference (ABS-HI) was in turn higher when the monkeys were hanging or bipedal than when they were quadrupedal. The strength of manual preference was higher for both the bimanual and experimental tasks than for unimanual tasks and spontaneous activities. Although our sample was too small to allow us to make any generalizations concerning lateral preferences in red-capped mangabeys, we propose some hypotheses about the influence of posture stability and task complexity.     

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.     

Tube task hand preference in captive hylobatids

The link between laterality in humans and other primates is still hotly debated. Hylobatids have been rather neglected in this research area, yet they can provide important insights because: (1) they share with humans a complex vocal repertoire, which in humans is thought to be associated with brain hemispheric specialization and lateralized behaviors; (2) their adaptation to arboreality has produced unique postural constraints; (3) the little that is known about laterality in gibbons is contradictory (captive studies have provided conflicting results, while a field study on siamangs reported a population-level left-hand preference). To clarify this, we investigated hand preference in captive hylobatids [n = 42; 22 siamangs (Symphalangus syndactylus) and 20 gibbons (Hylobates sp., Nomascus leucogenys)] in nine Japanese facilities. We had a large sample size, controlled for possible confounds (posture, enclosure limitations) and used a well-established testing protocol (tube task). Handedness indices calculated from raw frequencies and bouts were highly correlated and showed a significant left-hand skew, which is consistent with data from wild siamangs. Major differences between captive and wild siamangs were a larger number of ambiguously handed individuals, and no significant age-related variation in captivity. The use of the index finger elicited a much more strongly lateralized response than the thumb. These results confirmed a left-hand preference in siamangs, but were equivocal in other hylobatids, and suggest selective pressures that may have acted on the highly arboreal hylobatids to favor handedness. Our study also indicates factors that might explain the discrepancy in the literature between handedness studies on captive and wild primate populations.     

A Comparative Assessment of Hand Preference in Captive Red Howler Monkeys,Alouatta seniculus and Yellow-Breasted Capuchin Monkeys,Sapajus xanthosternos

There are two major theories that attempt to explain hand preference in non-human primates–the ‘task complexity’ theory and the ‘postural origins’ theory. In the present study, we proposed a third hypothesis to explain the evolutionary origin of hand preference in non-human primates, stating that it could have evolved owing to structural and functional adaptations to feeding, which we refer to as the ‘niche structure’ hypothesis. We attempted to explore this hypothesis by comparing hand preference across species that differ in the feeding ecology and niche structure: red howler monkeys, Alouatta seniculus and yellow-breasted capuchin monkeys, Sapajus xanthosternos. The red howler monkeys used the mouth to obtain food more frequently than the yellow-breasted capuchin monkeys. The red howler monkeys almost never reached for food presented on the opposite side of a wire mesh or inside a portable container, whereas the yellow-breasted capuchin monkeys reached for food presented in all four spatial arrangements (scattered, on the opposite side of a wire mesh, inside a suspended container, and inside a portable container). In contrast to the red howler monkeys that almost never acquired bipedal and clinging posture, the yellow-breasted capuchin monkeys acquired all five body postures (sitting, bipedal, tripedal, clinging, and hanging). Although there was no difference between the proportion of the red howler monkeys and the yellow-breasted capuchin monkeys that preferentially used one hand, the yellow-breasted capuchin monkeys exhibited an overall weaker hand preference than the red howler monkeys. Differences in hand preference diminished with the increasing complexity of the reaching-for-food tasks, i.e., the relatively more complex tasks were perceived as equally complex by both the red howler monkeys and the yellow-breasted capuchin monkeys. These findings suggest that species-specific differences in feeding ecology and niche structure can influence the perception of the complexity of the task and, consequently, hand preference.     

Hand Preference for a Novel Bimanual Coordinated Task During Termite Feeding in Wild Western Gorillas (<Emphasis Type="Italic">Gorilla gorilla gorilla</Emphasis>)

Although the level of handedness in humans varies cross-culturally, humans are generally described as right-handed, which has been considered a uniquely human trait. Recently, captive chimpanzees (Pan troglodytes) have been shown to exhibit right-hand preference when performing bimanual but not unimanual tasks. Less clear is whether this pattern also occurs in wild chimpanzees and other African apes. Using videos (N = 49) of six wild western gorillas (Gorilla gorilla gorilla) feeding on termites at the Mondika Research Center (Republic of Congo), we tested whether they exhibit hand preference when performing unimanual, i.e., reaching for termite mound pieces; bimanual, i.e., “termite tapping”: rhythmically shaking a piece of termite mound with the dominant hand and collecting the termites in the other hand tasks; or hand transfer prior to bimanual tasks, i.e., transferring a piece of termite mound from one hand to the other. All individuals exhibited exclusive hand preference when performing the bimanual tasks, with five of six gorillas preferring the right hand. Conversely, most individuals did not show any manual preference during the unimanual task. In addition, hand preference during hand transfer revealed clear hand dominance of similar strength and direction of those shown for the bimanual task, suggesting that this measure is as sensitive as the bimanual task itself. Thus, we propose “termite feeding” as a novel task to be considered in future hand-preference studies in wild western gorillas. Our results are in concordance with those for chimpanzees and captive gorillas showing hemispheric specialization for bimanual actions in apes.     

Hand preferences in captive gorillas,orang-utans and gibbons

Hand preference was assessed in 12 gorillas (Gorilla gorilla gorilla), 13 orang-utans (Pongo pygmaeus abelii), and 9 gibbons (Hylobates lar) by using a floor retrieval task and a mesh retrieval task. Hand preference was also assessed in 8 gorillas and 8 orang-utans by using a task involving the unfastening of a hasp. A bipedal requirement during testing (mesh retrieval task) facilitated detection of hand preferences. A significant left-hand preference was found for the gibbons with 6 of 6 gibbons preferring their left hand on the mesh retrieval task. Similarly, a significant right-hand preference was found for the gorillas with 10 of 12 gorillas preferring their right hand on the mesh retrieval task. The data for the orang-utan suggest a bimodal distribution on all tasks. Since the gibbon and gorilla in the wild engage in bipedal locomotion more frequently than the orangutan, one possible interpretation for these results correlates the degree of bipedal behavior of a species in its natural environment with its readiness to exhibit a unilateral population-level hand preference.     

Handedness in nature: first evidence on manual laterality on bimanual coordinated tube task in wild primates

Handedness is a defining feature of human manual skill and understanding the origin of manual specialization remains a central topic of inquiry in anthropology and other sciences. In this study, we examined hand preference in a sample of wild primates on a task that requires bimanual coordinated actions (tube task) that has been widely used in captive primates. The Sichuan snub-nosed monkey (Rhinopithecus roxellana) is an arboreal Old World monkey species that is endemic to China, and 24 adult individuals from the Qinling Mountains of China were included for the analysis of hand preference in the tube task. All subjects showed strong individual hand preferences and significant group-level left-handedness was found. There were no significant differences between males and females for either direction or strength of hand preference. Strength of hand preferences of adults was significantly greater than juveniles. Use of the index finger to extract the food was the dominant extractive-act. Our findings represent the first evidence of population-level left-handedness in wild Old World monkeys and broaden our knowledge on evaluating primate hand preference via experimental manipulation in natural conditions.     

Visual preference in a human-reared agile gibbon (<Emphasis Type="Italic">Hylobates agilis</Emphasis>)

Visual preference was evaluated in a male agile gibbon. The subject was raised by humans immediately after birth, but lived with his biological family from one year of age. Visual preference was assessed using a free-choice task in which five or six photographs of different primate species, including humans, were presented on a touch-sensitive screen. The subject touched one of them. Food rewards were delivered irrespective of the subject’s responses. We prepared two types of stimulus sets. With set 1, the subject touched photographs of humans more frequently than those of other species, recalling previous findings in human-reared chimpanzees. With set 2, photographs of nine species of gibbons were presented. Chimpanzees touched photographs of white-handed gibbons more than those of other gibbon species. The gibbon subject initially touched photographs of agile gibbons more than white-handed gibbons, but after one and two years his choice patterns resembled the chimpanzees’. The results suggest that, as in chimpanzees, visual preferences of agile gibbons are not genetically programmed but develop through social experience during infancy.     

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.     

Fecal Glucocorticoid Measurements and Their Relation to Rearing,Behavior, and Environmental Factors in the Population of Pileated Gibbons (<Emphasis Type="Italic">Hylobates pileatus</Emphasis>) Held in European Zoos

Pileated gibbons (Hylobates pileatus) are rated as endangered according to the International Union of Conservation of Nature (IUCN) Red List. The captive population suffers from poor breeding success and is threatened to become overaged. Although several factors are likely to contribute to the poor breeding success, one in particular may be chronic stress associated with prolonged periods of high glucocorticoid (GC) output. We investigated fecal GC levels of pileated gibbons (Hylobates pileatus) and their relationship to specific life-history variables and environmental factors. After validation of an enzyme immunoassay for the measurement of 5-reduced 3α,11β-dihydroxy cortisol metabolites to assess GC output reliably in pileated gibbons, we collected fecal samples over several days from all 36 European adult pileated gibbons located in 11 institutions and compared GC levels to intrinsic individual parameters, husbandry, behavior, and breeding history. Age, sex, and origin (wild vs. captive born) had no effect on GC levels. However, unnaturally reared gibbons had higher GC levels and showed more behavioral abnormalities than parent-reared individuals. Further, nonreproducing gibbons living in a pair without infants had higher GC concentrations than gibbons living in a family, bachelor group, or as singletons. With respect to environmental factors, a large size of the inside enclosure and the existence of visual protection from visitors was associated with lower fecal GC output. The data indicate that rearing and housing conditions appear to correlate to GC levels in pileated gibbons housed under captive conditions. It is hoped this knowledge will support the future management of the species in captivity and thus lead to a more successful breeding of this endangered primate.     

The potential effects of sex,posture and living condition on lateralized behaviors in ring-tailed lemurs (<Emphasis Type="Italic">Lemur catta</Emphasis>)

This research explores the effects of posture, sex, and living condition on hand and side preferences of semi-free-ranging, adult ring-tailed lemurs (Lemur catta) housed at the Duke University Primate Center in Durham, NC. Data were collected on 11 adult individuals (five females and six males) during normal daily activities over a ten-week period from May–July 2001. Variables analyzed in this study include unimanual behaviors (i.e., reach, hold, and limb used to start locomotion) and other potentially lateralized behaviors that do not involve handuse (i.e., whole-body turning and tail position). The data were analyzed to investigate potential individual and population level side biases for each behavior; potential sex biases in side preference for each behavior; and for ‘reach’, potential effects of posture (sitting, tripedal stance, or bipedal stance) on individual hand preferences. Additionally, to investigate potential effects of living condition on lateral biases, the data from this study were compared to data collected on the same individual Lemurs living under more restrictive living conditions during the previous year. Largely, as predicted based on available literature, we found that there was a significant sex difference across all hand-use categories and for whole-body turning, and that posture was a significant factor in the expression of hand preference for reaching. Contrary to previous research, the effect of living condition on lateral preferences was minimal, and no side preferences were found at the population level for any of the behaviors analyzed.     

Arboreal Postures Elicit Hand Preference when Accessing a Hard-to-Reach Foraging Device in Captive Bonobos (<Emphasis Type="Italic">Pan paniscus</Emphasis>)

Arboreal, and in particular suspensory, postures may elicit a preference for the strongest limb to be used in postural support in large bodied primates. However, selection may have favored ambilaterality rather than a preference for a particular hand in chimpanzees (Pan troglodytes) fishing arboreally for ants. To investigate the influence of arboreality on hand preference we recorded handedness in seven captive bonobos (Pan paniscus) manipulating a foraging device during terrestrial and arboreal postures in a symmetrical environment, observing 2726 bouts of manipulation. When accessing the foraging device in the arboreal position the bonobos adopted predominantly suspensory postures. There was no population level hand preference for manipulating the foraging device in either the terrestrial or arboreal positions. However, four of seven individuals that interacted with the foraging devices showed a significant preference for one hand (two were left handed, two were right handed) when manipulating the foraging device in the arboreal position whereas only one individual (left handed) showed a preference in the terrestrial position. This suggests that individuals may have a preferred or strongest limb for postural support in a symmetrical arboreal environment, resulting in a bias to use the opposite hand for manipulation. However, the hand that is preferred for postural support differs between individuals. Although our sample is for two captive groups at the same zoo, our findings suggest that the demand of maintaining arboreal postures and environmental complexity influence hand preference.     

Patterns and laterality of hand use in free-ranging aye-ayes (<Emphasis Type="Italic">Daubentonia madagascariensis</Emphasis>) and a comparison with captive studies

We observed hand use in free-ranging aye-ayes (Daubentonia madagascariensis) on an island in the Mananara River, eastern Madagascar. The results were compared with those of two conflicting studies on hand laterality in captive aye-ayes. We argue that patterns of hand preference in wild aye-ayes are comparable to those of captive animals and that discrepancies between studies are—at least partly—caused by different ways of collecting and processing data. Aye-ayes fit Level 2 of the categories of hand laterality described by McGrew and Marchant (Yearb Phys Anthropol 40:201–232, 1997), with some individuals showing significant hand preference, but with the proportion of right- to left-preferent animals being very close to 1:1. We observed hand preference to be consistent for two of the most frequent behaviors, tapping and probing with fingers. Reaching and holding objects in hands is rare in aye-ayes, and the patterns of hand use in aye-ayes are therefore not directly comparable with those of other prosimians in which laterality has been studied. We detected no effect of sex on hand preference and were unable to determine whether there is an effect of age. The posture adopted by the animals did not influence hand preference.     

A study of correlates of hand preferences in squirrel monkeys (Saimiri sciureus)

The purpose of this study was to test the influence of sex, age, social rank, matriline membership, posture, and visual and tactual motor control on manual preferences inSaimiri sciureus. A well-established social group of 12 squirrel monkeys, aged 2 to 14 yrs and consisting of two matrilines with social rank known for each animal, was presented with four different food-reaching tasks and assessed for hand preferences with a minimum of 100 reaches per animal. Frequency of occurrence of hand preferences at the group level and degree of hand preferences at the individual level depended on posture and on whether the reaching act took place under visual or tactual guidance. Sex, age, social rank, and matriline membership were not found to determine frequency of occurrence, direction or degree of hand preferences with the exception of one task in which a significant negative correlation between the degree of hand preference and age was found. Nine out of 12 monkeys showed task-dependent changes in the hand they used preferentially while only three animals preferred the same hand in all four tasks. Significant preferences for the use of right or left hand on a given task were distributed almost equally between individuals. Thus, the results of this study suggest task-specific demands like posture and/or whether reaching was visually or tactually guided to be the major correlates of hand preferences in food-reaching tasks in squirrel monkeys.     

Food Preferences and Nutrient Composition in Captive White-handed Gibbons, <Emphasis Type="Italic">Hylobates lar</Emphasis>

We aimed to assess spontaneous food preferences in captive white-handed gibbons and to analyze whether they correlate with nutrient composition. Via a 2-alternative choice test, we repeatedly presented 3 male Hylobates lar with all possible binary combinations of 10 types of food that are part of their diet in captivity and found the following rank order of preference: grape > banana = fig > apple > pear > honeydew melon > carrot > tomato > cucumber > avocado. Correlational analyses revealed a highly significant positive correlation between the food preference ranking and the total carbohydrate, fructose, and glucose contents of the foods (p < 0.01, respectively). With the exception of the trace mineral selenium (p < 0.05), there was no other significant correlation with any other macro- or micronutrient. In addition, the food preferences were stable across the day because rankings obtained from tests performed at 0900, 1200, and 1500 h, respectively, did not differ significantly (p > 0.05). Our results suggest that captive white-handed gibbons are not opportunistic, but selective feeders with regard to maximizing net gain of energy because only the content of carbohydrates, but not the contents of total energy, proteins, or lipids significantly correlate with the displayed food preferences. Further, the results suggest that captive Hylobates lar, in contrast to their free-ranging conspecifics, do not display marked changes in their food selection across the day.     

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.     

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 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.     

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.