Laterality in great apes
Laterality in non-human primates has traditionally been considered bimodal, that is, a population would divide equally into right-handed and left-handed individuals. Warren (1980) proposed that individual hand preferences were due to random experiential or environmental factors, or both, rather than to an underlying specialization of the contralateral hemisphere.
Nevertheless, a good number of later studies have evidenced the influence of posture on the strength of laterality between species. An interesting theory in this sense is that of MacNeilage et al. (1987), later known as the postural origins theory (MacNeilage,1991), according to which hand preference evolved among primitive arboreal species from a right-hand preference for visuo-spatial tasks and a left-hand preference for reaching or manual predation on insects. When among terrestrial species postural constraints were less pronounced, left-handedness remained dominant for reaching while the right hand was preferred for manipulation.
The present article does not intend to give a detailed account of all the studies that have been carried out in this field - this will be left to the curious reader - but to centre mainly on the work done by William D. Hopkins (Emory University, Atlanta, Georgia) with the chimpanzees, orangutans and bonobos at the Yerkes Primate Research Center, and studies carried out in the wild on great ape species ( Byrne & Byrne, 1991; Sugiyama et al., 1993; M.C. McGrew and L.F. Marchant (1999).
One experiment (Hopkins, W.D., 1993), involving 40 chimpanzees (16 males, 24 females) ranging from 3.8 to 37.9 years, and 9 orangutans (7 males, 2 females) from 4.2 to 18.8 years of age, studied the influence of quadrupedal or bipedal posture on hand preference (left, right or non-preferent) for reaching. An analysis of hand preference is based on the subject´s preferential use of one hand for a single task (Mc Grew M.C. & Marchant L.F., 1993).
For quadrupedal posture the chimpanzees gave a distribution that did not differ from chance: 12 left-handed, 11 right-handed and 17 non-preferent. However, for bipedal posture, there were 6 left-handed individuals, 28 right-handed and 6 non-preferent. In an analysis for difference between the sexes, the results were not significant for quadrupedal posture but were clearly significant for bipedal posture: 61% of the males showed a right-hand preference, while for females it was an 85%.
An analysis of variance evidenced a greater percentage of right-hand use in bipedal reaching for nursery-reared individuals (63%) than for mother-reared (49%).
For the 9 orangutans the results were similar, for upright reaching a right-hand preference was found.
Hopkins carried out a second experiment on 140 captive chimpanzees, 59 males and 81 females ranging from 3 to 55 years of age, 60 of whom were mother-reared, to assess hand preference for bimanual feeding (Hopkins, W.D., 1994).This experiment continued over a period of sixty days and, for statistical purposes, the individuals were divided into three age groups: juveniles and sub-adults from 3 to 10 years of age (23 females, 18 males), young adults from 11 to 22 (24 females, 28 males), and older adults over 22 (34 females, 13 males).
Hand use was recorded only when the individuals were seen feeding with one hand for a minimum of 3 seconds while holding the remaining food in the opposite hand.
The data were measured on the percentage of right-hand use in feeding, on the absolute strength in lateral bias, and on a classification of each individual as being right-handed, left-handed or non-preferent, according to the number of right or left hand responses. An individual was considered as having a left or right hand bias depending on whether the left or right hand was used for feeding while the opposite hand held the remaining food.
The results reflect a clear direction of hand preference: 54 right-handed individuals, 28 left-handed and 58 non-preferent. However, the chi-square comparison between mother-reared or nursery-reared and the direction of hand preference was not significant, nor were the comparisons sex/hand-preference or age group/hand-preference.
On the other hand, when overall strength in hand preference was analyzed, the results were significant for rearing: mother-raised individuals were more lateralized than the nursery reared, and for age: juveniles were less lateralized than both young and older adults.
A study involving 44 free-ranging gorillas (Byrne & Byrne, 1991) and a previous study by Hopkins involving 21 captive bonobos (Hopkins et al, 1993) reported right-handedness at a population level for bimanual feeding, that is, the hand preference found for the task was consistent across most subjects involved in the study (McGrew, W.C. & Marchant L.F., 1993).
A later study (Hopkins, W.D. & Fernández-Carriba, S., 2000) on hand preference for feeding support the previous findings, giving a 67% right-hand bias.
Since the majority of previous studies had been based on unimanual action, which can be influenced by postural and/or situational factors, or on tasks recorded as being bimanual but somewhat equivocal in their interpretation, Hopkins decided to perform a third experiment (Hopkins, W.D., 1995) based on a coordinated bimanual task for the purpose of minimizing the influence of postural or situational factors and in the hope that it might elicit stronger hand preferences than a bimanual feeding task, which involves independent actions of the two hands. Also special interest was placed on detecting variability in the strength and/or direction of hand preference between age groups.
The study was done on 110 chimpanzees (45 males and 65 females), ranging from 3 to 54 years of age and classified into 3 age groups: 23 juveniles (12 females and 11 males), 30 adolescents (11 females and 19 males), and 57 adults (42 females and 15 males). 47 individuals were mother reared and 63 nursery reared.
The task consisted in presenting the subjects with PVC tubes 24 to 31 cm. in length and 4 cm. in diameter, coated with peanut butter at approximately 7 cm. from the inside edge of the tube. The tubes were passed through the cage mesh -the hand used by the experimenter being randomly determined- to the members of the group, but only one individual was the focal subject each time. Each individual was tested twice and sessions were separated by 2 to 24 days.
The data collected were divided into the hand and the digit used to remove the peanut butter. For the direction of hand preference, the results differed significantly from chance: 59 right-handed, 32 left-handed, and 19 non-preferent. No significant differences were found between sexes, rearing conditions, or age groups.
However, for strength in hand preference, adults were significantly more lateralized than adolescents and juveniles. Use of the index finger to extract the peanut butter reached a 90% among adult chimpanzees. Right-handed index finger responses were significantly higher than all other hand and digit comparisons.
The study on behavioural laterality in captive bonobos (Hopkins W.D. et al., 1993) was done mainly to investigate stronger degrees of hemispheric specialization because they walk bipedally more frequently than chimpanzees and, according to some (Savage-Rumbaugh et al, 1986), they possess more advanced linguistic capacities than other great ape species.
Eleven bonobos, 5 males and 6 females, ranging from 2 to 42 years of age were videotaped for a total of 14 hours 15 minutes at the Yerkes Main Center for the purpose of studying 7 types of behaviour: feeding, reaching, self-touching, face touching, carrying, gesture and leading limb to measure the frequency of left- and right-hand use.
In the case of carrying and leading limb, quadrupedal and bipedal postures were also recorded. The significant results can be summarized as follows: there was a right-hand preference for feeding while holding remaining food with the left hand; older individuals showed more consistent right-hand preference in feeding than did younger subjects; bipedal posture tended to increase left-hand preference in carrying and right side preference for leading limb; a significant relation between reaching and leading limb was found; for quadrupedal and upright posture right-hand use gave a mean percentage of 53.8% and 71%, respectively.
The previous experiments were carried out on captive individuals of diverse origin, a good number of whom were born in captivity. The following study also analyzed hand preference but aimed at measuring foraging success among free-ranging chimps in Gombe, Tanzania while fishing for termites (McGrew, W.C. & Marchant, L.F., 1999).
The individuals were classified into two groups: those who showed preference for one hand, whether left or right, and those who were non-preferent. The subjects were observed from a distance of 3 to 5 meters. The data recorded included, among other items, the number of major soldier termites consumed each time the feeding tool was extracted from the mound.
Of the 16 individuals (9 males and 7 females) that concluded the experiment, 11 were adults and 5 sub-adults. 8 fished with the left hand, 2 with the right, 3 were incompletely lateralized, and 3 were non-preferent.
The chimpanzees who were 100% lateralized obtained 38% more soldier termites per minute and 36% more termites per withdrawal. The results evidence the fact that the completely lateralized individuals were more successful at an extractive foraging task but the findings obviously do not support a right-hand preference among the population.
A later study was done (Hopkins et al. 2003) on tool use, but among captive chimpanzees. The task emulated termite fishing in the wild. The results support prior findings on captive chimps performing coordinated bimanual tasks, mainly a population level right-handedness.
Finally, mention should be made of the study done on an habituated but non-provisioned group of 17 wild chimpanzees at Bossou, Republic of Guinea by Sugiyama et al. (1993). Two different types of behaviour were examined: picking food from a branch and putting it into the mouth, and cracking hard nuts using a hammer and an anvil.
For food picking, left-hand/right-hand bias measured from the number of feeding bouts was not significant at the population level, although there was individual hand preference as regards the number of food pickings (9 right-hand individuals, 3 left-hand and 6 non-preferent). A clear correlation was found between hand preference for food picking and for hammer holding. No right-hand/left-hand discrepancy existed.
Among adults, 5 used only the left hand and 3 only the right hand for holding the hammer. However, when the adolescents, juveniles and infants were included in the analysis, the total number of right-hand users increased to 8, and left-hand users to 6, indicating a strong, almost exclusive, hand preference at the individual level, but no left/right bias at the population level.
Handedness at a population level - the predominant use of one hand is consistent across most subjects and most tasks (McGrew, W.C. & Marchant L.F., 1993) - has traditionally been considered privative of humans. However, recent studies report a certain bias in laterality within and between different non-human primate species.
Although hand preference seems to be incompletely developed until adulthood, a population right-hand bias for bipedal reaching has been found in captive bonobos, chimpanzees, orangutans and gorillas. A right-hand bias has also been reported for bimanual feeding in captive bonobos, chimpanzees and in free-ranging gorillas, and for bimanual manipulation in captive chimps for which they displayed an even higher degree of lateralization than for bimanual feeding.
However, a clear left-hand bias has been found in captive bonobos for carrying and in free-ranging chimpanzees for extractive foraging. Among the adult chimpanzees at Bossou, Republic of Guinea, an exclusive hand preference was found for tool use, more than 50% being left-handed.
Although it is not possible to draw any definite conclusions based on these findings due, in part, to the dissimilarity of the tasks and measures employed on different species; nevertheless, it can be said that the data strongly point toward the existence of an individual or within subject lateral bias but not necessarily an overall common direction in hand preference within and between different non-human primate species.
Byrne, R.W. & Byrne, J.M. (1991). Hand Preferences in the Skilled Gathering tasks of Mountain Gorillas (Gorilla gorilla berengei) in Cortex, 27:521-536.
Corballis, M.C. (1997). The Genetics and Evolution of Handedness in Psychological Review 104 (4): 714-727.
Hopkins, W.D. (1993). Posture and Reaching in Chimpanzees (Pan troglodytes) and Orangutans (Pongo pygmaeus) in Journal of Comparative Psychology, 107 (2): 162-168.
Hopkins, W.D., Bennett, A.J., Bales, S.L., Lee, J. & Ward, J.P. (1993). Behavior Laterality in Captive Bonobos (Pan paniscus) in Journal of Comparative Psychology, 107 (4): 403-410.
Hopkins, W.D. (1994). Hand Preferences for Bimanual Feeding in 140 Captive Chimpanzees (Pan troglodytes): Rearing and Ontogenetic Determinants in Developmental Psychobiology 27, (6): 395-407.
Hopkins, W.D. (1995). Hand preferences for a Coordinated Bimanual Task in 110 Chimpanzees (Pan troglodytes): Cross-Sectional Analysis in Journal of Comparative Psychology, 109 (3): 291-297.
Hopkins, W.D. & Fernández-Carriba, S. (2000). The Effect of Situational Factors on Hand Preferences for Feeding in 177 Captive Chimpanzees (Pan troglodytes) in Neuropsicología, 38: 403-409.
Hopkins, W.D., Braccini, S.N., Hook, M.A. & Shapiro, S.J. Hand Preferences on a Tool-Using Task in a Large Sample of Chimpanzees (Pan troglodytes). ASP Conference 2003.
Mac Neilage, P.F., Studdert-Kennedy, M.G. & Lindblom, B. (1987). Primate Handedness Reconsidered in Behavioral and Brain Sciences, 10: 247-303.
MacNeilage, P.F. (1991). The ` Postural Origins´ Theory of Primate Neurobiological Asymmetries in Biological and Behavioral Determinants of Language Development (pp. 165-188). Krasnegor, N.A., Rumbaugh, D.M., Schiefelbusch, R.L. & Studdert-Kennedy, M. (Eds.). Hillsdale, N.J.: Erlbaum.
McGrew, W.C. & Marchant, L.F. (1993). Primate Ethology: a Perspective on Human and Non-human Handedness in Handbook of Psychological Anthropology, P.K. Bock (ed.9, Greenwood Press, Westport.
McGrew, W.C. & Marchant, L.F. (1999). Laterality of Hand Use Pays Off in Foraging Success for Wild Chimpanzees in Primates, 40 (3): 509-513.
Savage-Rumbaugh, E.S., McDonald, K., Sevcik, R.A., Hopkins, W.D. & Rupert, E. (1986). Spontaneous Symbol Acquisition and Communicative Use by Two Pygmy Chimpanzees in Journal of Experimental Psychology: General, 115, 211-235.
Sugiyama, Y., Fushimi, T., Sakura, O. & Matsuzawa, T. (1993). Hand Preference and Tool Use in Wild Chimpanzees in Primates, 34 (2): 151-159.
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