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


Affiliations
1 Department of Psychology, University of Georgia, Athens, GA 30602, United States
2 Indian Institute of Science Education and Research, Pune 411 008, India
3 Biopsychology Laboratory, and Institute of Excellence, University of Mysore, Mysore 570 006, India
 

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.

Keywords

Division of Labour, Hand Performance and Preference, Laterality, Manual Asymmetry, Non-Human Primates.
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  • Mangalam, M., Desai, N. and Singh, M., Division of labor in hand usage in free-ranging bonnet macaques, Macaca radiata. Am. J. Primatol., 2014, 76, 576–585.

  • Mangalam, M., Desai, N. and Singh, M., Division of labor in hand usage is associated with higher hand performance in free-ranging bonnet macaques, Macaca radiata. PLoS ONE, 2015, 10, e0119337.

  • Bradshaw, J. and Rogers, L. J., The Evolution of Lateral Asymmetries, Language, Tool Use and Intellect, Academic Press, San Diego, 1993.

  • Papademetriou, E., Sheu, C. F. and Michel, G. F., A meta-analysis of primate hand preferences, particularly for reaching. J. Comp. Psychol., 2005, 119, 33–38.

  • Ward, J. P. and Hopkins, W. D., Primate Laterality: Current Behavioral Evidence of Primate Asymmetries, Springer-Verlag, New York, NY, 1993.

  • MacNeilage, P. F., Studdert-Kennedy, M. J. and Lindblom, B., Primate handedness reconsidered. Behav. Brain Sci., 1987, 10, 247–263.

  • McGrew, W. C. and Marchant, L. F., On the other hand: current issues in and meta-analysis of the behavioral laterality of hand function in nonhuman primates. Yearb. Phys. Anthropol., 1997, 40, 201–232.

  • Fagot, J. and Vauclair, J., Manual laterality in nonhuman primates: a distinction between handedness and manual specialization. Psychol. Bull., 1991, 109, 76–89.

  • Mangalam, M. and Singh, M., Flexibility in food extraction techniques in urban free-ranging bonnet macaques, Macaca radiata. PLoS ONE, 2013, 8, e85497.

  • Witelson, S. F., Hand preference: basis or reflection of hemispheric specialization? Behav. Brain Sci., 1988, 11, 735–736.

  • Fragaszy, D. M. and Mitchell, S. R., Hand preference and performance on unimanual and bimanual tasks in capuchin monkeys (Cebus apella). J. Comp. Psychol., 1990, 104, 275–282.

  • Lilak, A. L. and Phillips, K. A., Consistency of hand preference across low‐level and high‐level tasks in Capuchin monkeys (Cebus apella). Am. J. Primatol., 2008, 70, 254–260.

  • Meunier, H. and Vauclair, J., Hand preferences on unimanual and bimanual tasks in white‐faced capuchins (Cebus capucinus). Am. J. Primatol., 2007, 69, 1064–1069.

  • Spinozzi, G., Castorina, M. G. and Truppa, V., Hand preferences in unimanual and coordinated-bimanual tasks by tufted capuchin monkeys (Cebus apella). J. Comp. Psychol., 1998, 112, 183–191.

  • Westergaard, G. C., Kuhn, H. E., Lundquist, A. L. and Suomi, S. J., Posture and reaching in tufted capuchins (Cebus apella). Laterality, 1997, 2, 65–74.

  • Parr, L. A., Hopkins, W. D. and de Waal, F. B. M., Haptic discrimination in capuchin monkeys (Cebus apella): evidence of manual specialization. Neuropsychologia, 1996, 35, 143–152.

  • Garber, P. A., Gomes, D. F. and Bicca-Marques, J. C., Experimental field study of hand preference in wild black-horned (Cebus nigritus) and white-faced (Cebus capucinus) capuchins: evidence for individual and species differences. Anim. Cogn., 2008, 11, 401–411.

  • Westergaard, G. C., Kuhn, H. E. and Suomi, S. J., Effects of upright posture on hand preference for reaching vs the use of probing tools by tufted capuchins (Cebus apella). Am. J. Primatol., 1998, 44, 147–153.

  • Westergaard, G. C. and Suomi, S. J., Hand preference in capuchin monkeys varies with age. Primates, 1993, 34, 295–299.

  • Spinozzi, G., Truppa, V. and Lagana, T., Grasping behavior in tufted capuchin monkeys (Cebus apella): grip types and manual laterality for picking up a small food item. Am. J. Phys. Anthropol., 2004, 125, 30–41.

  • Westergaard, G. C. and Suomi, S. J., Capuchin monkey (Cebus apella) grips for the use of stone tools. Am. J. Phys. Anthropol., 1997, 103, 131–135.

  • Westergaard, G. C. and Suomi, S. J., Hand preference for a bimanual task in tufted capuchins (Cebus apella) and rhesus macaques (Macaca mulatta). J. Comp. Psychol., 1998, 110, 406–411.

  • Spinozzi, G., Lagana, T. and Truppa, V., Hand use by tufted capuchins (Cebus apella) to extract a small food item from a tube: digit movements, hand preference, and performance. Am. J. Primatol., 2007, 69, 336–352.

  • Spinozzi, G. and Truppa, V., Problem-solving strategies and hand preferences for a multicomponent task by tufted capuchins (Cebus apella). Int. J. Primatol., 2002, 23, 621–638.

  • Spinozzi, G. and Cacchiarelli, B., Manual laterality in haptic and visual reaching tasks by tufted capuchin monkeys (Cebus apella): an association between hand preference and hand accuracy for food discrimination. Neuropsychologia, 2000, 38, 1685–1692.

  • Lacreuse, A. and Fragaszy, D. M., Manual exploratory procedures and asymmetries for a haptic search task: a comparison between capuchin monkeys (Cebus apella) and humans. Laterality, 1997, 2, 247–266.

  • Lacreuse, A. and Fragaszy, D. M., Hand preferences for a haptic searching task by tufted capuchins (Cebus apella). Int. J. Primatol., 1996, 17, 613–632.

  • Lacreuse, A., Left hand preferences in capuchins (Cebus apella): role of spatial demands in manual activity. Laterality, 1999, 4, 65–78.

  • Wilson, M., Tactual discrimination learning in monkeys. Neuropsychologia, 1965, 3, 353–361.

  • Westergaard, G. C. and Suomi, S. J., The use of probing tools by tufted capuchins (Cebus apella): evidence for increased right-hand preference with age. Int. J. Primatol., 1994, 15, 521–529.

  • Westergaard, G. C., Kuhn, H. E. and Suomi, S. J., Laterality of hand function in tufted capuchin monkeys (Cebus apella): comparison between tool use actions and spontaneous non‐tool actions. Ethology, 1998, 104, 119–125.

  • Westergaard, G. C. and Suomi, S. J., Asymmetrical manipulation in the use of tools by tufted capuchin monkeys (Cebus apella). Folia Primatol., 1994, 63, 96–98.

  • Anderson, J. R., Degiorgio, C., Lamarque, C. and Fagot, J., A multi-task assessment of hand lateralization in capuchins (Cebus apella). Primates, 1996, 37, 97–103.

  • Westergaard, G. C., Hand preference in the use and manufacture of tools by tufted capuchin (Cebus apella) and lion-tailed macaque (Macaca silenus) monkeys. J. Comp. Psychol., 1991, 105, 172–176.

  • Westergaard, G. C. and Suomi, S. J., Hand preference in the use of nut-cracking tools by tufted capuchin monkeys (Cebus apella). Folia Primatol., 1993, 61, 38–42.

  • Westergaard, G. C. and Suomi, S. J., Hand preference for stone artefact production and tool-use by monkeys: possible implications for the evolution of right-handedness in hominids. J. Hum. Evol., 1996, 30, 291–298.

  • Panger, M. A. and Wolfe, L. D., Carrying and hand-use patterns in Panamanian white-faced capuchins (Cebus capucinus). Primates, 2000, 41, 407–411.

  • Westergaard, G. C., Haynie, M. K., Lundquist, A. L. and Suomi, S. J., Carrying, sharing, and hand preference in tufted capuchins (Cebus apella). Int. J. Primatol., 1999, 20, 153–162.

  • Hopkins, W. D., Laterality in maternal cradling and infant positional biases: implications for the development and evolution of hand preferences in nonhuman primates. Int. J. Primatol., 2004, 25, 1243–1265.

  • Porter, R., The corticomotoneuronal component of the pyramidal tract: corticomotoneuronal connections and functions in primates. Brain Res., 1985, 1, 1–26.

  • Elliott, D. and Chua, R., Manual asymmetries in goal-directed movement. In Manual Asymmetries in Motor Performance (eds Elliott, D. and Roy, E. A.), CRC Press, New York, NY, 1996, pp. 143–157.

  • Healey, J. M., Liederman, J. and Geschwind, N., Handedness is not a unidimensional trait. Cortex, 1986, 22, 33–53.

  • Steenhuis, R. E., Hand preference and performance in skilled and unskilled activities. In Manual Asymmetries in Motor Performance (eds Elliott, D. and Roy, E. A.), CRC Press, New York, NY, 1996, pp. 123–142.

  • Steenhuis, R. E. and Bryden, M. P., Different dimensions of hand preference that relate to skilled and unskilled activities. Cortex, 1989, 25, 289–304.

  • Sfar, N., Mangalam, M., Kaumanns, W. and Singh, M., A comparative assessment of hand preference in captive red howler monkeys, Alouatta seniculus and yellow-breasted capuchin monkeys, Sapajus xanthosternos. PLoS ONE, 2014, 9, e107838.

  • Napier, J. R., The prehensile movements of the human hand. J. Bone Joint Surg., 1956, 38, 902–913.

  • Napier, J. R. and Napier, P. H., A Handbook of Living Primates, Academic Press, London, UK, 1967.

  • Bishop, A., Use of the hand in lower primates. In Evolutionary and Genetic Biology of the Primates (ed. Buettner, J. J.), Academic Press, New York, NY, 1964, pp. 133–225.

  • Napier, J. R., Hands, Princeton University Press, Princeton, New Jersey, 1993.

  • Fragaszy, D. M., Time budgets and foraging behavior in wedgecapped capuchins (Cebus olivaceus): age and sex differences. In Current Perspectives in Primate Social Dynamics (eds Taub, D. and King, F.), van Rostrand Reinhold, New York, NY, 1990, pp. 159–174.

  • Panger, M. A., Object-use in free-ranging white-faced capuchins (Cebus capucinus) in Costa Rica. Am. J. Phys. Anthropol., 1988, 106, 311–321.

  • Costello, M. B. and Fragaszy, D. M., Prehension in Cebus and Saimiri: I. Grip type and hand preference. Am. J. Primatol., 1988, 15, 235–245.

  • Christel, M. I. and Fragaszy, D. M., Manual function in Cebus apella. Digital mobility, preshaping, and endurance in repetitive grasping. Int. J. Primatol., 2000, 21, 697–719.

  • Muir, R. B. and Lemon, R. N., Corticospinal neurons with a special role in precision grip. Brain Res., 1983, 261, 312–316.

  • Kuypers, H. G. J. M., Anatomy of the descending pathways. In Handbook of Physiology, Section 1: The Nervous System II (eds Brookhart, V. B. V. and Mountcastle, J. M.), American Physiology Society, Bethesda, MD, 1981, pp. 597–666.

  • Lemon, R. N., Cortical control of the primate hand. Exp. Physiol., 1993, 78, 263–301.

  • Shinoda, Y., Yokota, J. L. and Futami, T., Divergent projection of individual corticospinal axons to motoneurons of multiple muscles in the monkey. Neurosci. Lett., 1981, 23, 7–21.

  • Bortoff, G. A. and Strick, P. L., Corticospinal terminations in two New-World primates: further evidence that corticoneuronal connections provide part of the neural substrate for manual dexterity. J. Neurosci., 1993, 13, 5105–5118.

  • Phillips, K. A. and Hopkins, W. D., Exploring the relationship between cerebellar asymmetry and handedness in chimpanzees (Pan troglodytes) and capuchins (Cebus apella). Neuropsychologia, 2007, 45, 2333–2339.

  • Phillips, K. A. and Sherwood, C. C., Primary motor cortex asymmetry is correlated with handedness in capuchin monkeys (Cebus apella). Behav. Neurosci., 2005, 119, 1701–1704.

  • Phillips, K. A., Sherwood, C. C. and Lilak, A. L., Corpus callosum morphology in capuchin monkeys is influenced by sex and handedness. PLoS ONE, 2007, 2, e792.

  • Phillips, K. A. and Sherwood, C. C., Cerebral petalias and their relationship to handedness in capuchin monkeys (Cebus apella). Neuropsychologia, 2007, 45, 2398–2401.

  • Vallortigara, G. and Rogers, L. J., Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav. Brain Sci., 2005, 28, 575–588.

  • Trehub, S. E., Manual specialization and the developing brain: an overview. In Manual Specialization and the Developing Brain (eds Young, G. et al.), Academic Press, New York, NY, 1983, pp. 257–274.


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

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Authors

Madhur Mangalam
Department of Psychology, University of Georgia, Athens, GA 30602, United States
Nisarg Desai
Indian Institute of Science Education and Research, Pune 411 008, India
Mewa Singh
Biopsychology Laboratory, and Institute of Excellence, University of Mysore, Mysore 570 006, India

Abstract


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.

Keywords


Division of Labour, Hand Performance and Preference, Laterality, Manual Asymmetry, Non-Human Primates.

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DOI: https://doi.org/10.18520/cs%2Fv110%2Fi9%2F1630-1638