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

Developmental Psychobiology

Volumn 55, Issue 6, 2013, Pages 621-636

  Hopkins, William D ^a,b  

^a GEORGIA STATE UNIVERSITY   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

Comparative analysis; Handedness; Laterality; Measurement validity; Primates

Indexed keywords

HAPLORHINI; PRIMATES;

ANIMAL; ARTICLE; BRAIN; COMPARATIVE ANALYSIS; HANDEDNESS; HEMISPHERIC DOMINANCE; HUMAN; MEASUREMENT VALIDITY; PHYSIOLOGY; PRIMATE;

COMPARATIVE ANALYSIS; HANDEDNESS; LATERALITY; MEASUREMENT VALIDITY; PRIMATES;

ANIMALS; BRAIN; FUNCTIONAL LATERALITY; HUMANS; PRIMATES;

EID: 84882277976     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.21139     Document Type: Article

References (102)

1. Annett, M. (1985). Left, right, hand, and brain: The right-shift theory. London: Lawrence Erlbaum Associates.
2. Aruguete, M. A., Ely, E. A., & King, J. E. (1992). Laterality in spontaneous motor activity of chimpanzees and squirrel monkeys. American Journal of Primatology, 27, 13-21.
3. Bennett, A. J., Suomi, S. J., & Hopkins, W. D. (2008). Effects of early adverse experiences on behavioral lateralisation in rhesus monkeys (Macaca mulatta). Laterality, 13(3), 282-292.
4. Biro, D., Inoue-Nakamura, N., Tonooka, R., Yamakoshi, G., Sousa, C., & Matsuzawa, T. (2003). Cultural innovation and transmission of tool use in wild chimpanzees: Evidence from field experiments. Animal Cognition, 6(4), 213-223.
5. Biro, D., Sousa, C., & Matsuzawa, T. (2006). Ontogeny and cultural propagation of tool use by wild chimpanzees at Bossou, Guinea: Case studies in nut cracking and leaf folding. In: T. Matsuzawa, T. Tomonaga, & M. Tanaka (Eds.), Cognitive development of chimpanzees (pp. 476-507). New York: Springer.
6. Boesch, C. (1991). Handedness in wild chimpanzees. International Journal of Primatology, 6, 541-558.
7. Bogart, S. L., Pruetz, J. D., Ormiston, L. K., Russell, J. L., Meguerditchian, A., & Hopkins, W. D. (2012). Termite fishing laterality in the Fongoli savanna chimpanzees (Pan troglodytes verus): Further evidence of a left hand preference. American Journal of Physical Anthropology, 149, 591-598.
8. Braccini, S., Lambeth, S. P., Schapiro, S. J., & Fitch, W. T. (2010). Bipedal tool use strengthens chimpanzee hand preferences. Journal of Human Evolution, 58, 234-241.
9. Bradshaw, B., & Rogers, L. (1993). The evolution of lateral asymmetries, language, tool-use and intellect. San Diego: Academic Press.
10. Byrne, R. W., & Byrne, J. M. (1991). Hand preferences in the skilled gathering tasks of mountain gorillas (Gorilla gorilla berengei). Cortex, 27, 521-536.
11. Cashmore, L. (2009). Can hominin "handedness" be accuartely assessed? Annals of Human Biology, 36(5), 624-641.
12. Cashmore, L., Uomini, N., & Chapelain, A. (2008). The evolution of handedness in humans and great apes: A review and current issues. Journal of Anthropological Sciences, 86, 7-35.
13. Chapelain, A., & Hogervorst, E. (2009). Hand preferences for bimanual coordination in 29 bonobos (Pan paniscus). Behavioural Brain Research, 196, 15-29.
14. Chapelain, A., Hogervorst, E., Mbonzo, P., & Hopkins, W. D. (2011). Hand preferences for bimanual coordination in 77 bonobos (Pan paniscus): Replication and extension. International Journal of Primatology, 32, 491-510.
15. Coren, S., Porac, C., & Duncan, P. (1981). Lateral preference behaviors in preschool children and young adults. Child Development, 52(2), 443-450.
16. Corp, N., & Byrne, R. W. (2004). Sex difference in chimpanzee handedness. American Journal of Physical Anthropology, 123, 62-68.
17. Crow, T. J. (2009). A theory of the origin of cerebral asymmetry: Epigenetic variation superimposed on a fixed right-shift. Laterality, 15(3), 289-303.
18. Dadda, M., Cantalupo, C., & Hopkins, W. D. (2006). Further evidence of an association between handedness and neuroanatomical asymmetries in the primary cortex of chimpanzees (Pan troglodytes). Neuropsychologia, 44, 2482-2486.
19. Diamond, A. C., & McGrew, W. C. (1994). True handedness in the Cotton-top tamarin (Saguinus oedipus)? Primates, 35(1), 69-77.
20. Ettlinger, G. F. (1988). Hand preference, ability and hemispheric specialization. How far are these factors related in the monkey? Cortex, 24, 389-398.
21. Fagard, J., & Marks, A. (2000). Unimanual and bimanual tasks and the assessment of handedness in toddlers. Developmental Science, 3(2), 137-147.
22. Fagot, J., Drea, C., & Wallen, K. (1991). Asymmetrical hand use in rhesus monkeys (Macaca mulatta) in tactually and visually regulated tasks. Journal of Comparative Psychology, 105, 260-268.
23. Forrester, G. S., Leavens, D. A., Quaresmini, C., & Vallortigara, G. (2011). Target animacy influences gorilla handedness. Animal Cognition, 14, 903-907.
24. Forrester, G. S., Quaresmini, C., Leavens, D. A., Mareschal, D., & Thomas, M. S. C. (2013). Human handedness: An inherited evolutionary trait. Behavioral Brain Research, 237, 200-206.
25. Forrester, G. S., Quaresmini, C., Leavens, D. A., Spiezio, C., & Vallortigara, G. (2012). Target animacy influences chimpanzee handedness. Animal Cognition, 15(6), 1121-1127.
26. Garber, P. A., Gomes, D. F., & Bicca-Marques, J. C. (2008). Experimental field study of hand preference in wild black-horned (Cebus nigritus) and white-faced (Cebus capucinus): Evidence for individual and species differences. Animal Cognition, 11(3), 401-411.
27. Hook-Costigan, M. A., & Rogers, L. J. (1997). Hand preferences in New World primates. International Journal of Comparative Psychology, 9, 173-207.
28. Hopkins, W. D. (1993). Posture and reaching in chimpanzees (Pan) and orangutans (Pongo). Journal of Comparative Psychology, 17, 162-168.
29. Hopkins, W. D. (1995). Hand preferences in juvenile chimpanzees: Continuity in development. Developmental Psychology, 31, 619-625.
30. Hopkins, W. D. (1999). On the other hand: Statistical issues in the assessment and interpretation of hand preference data in non-human primates. International Journal of Primatology, 20, 851-866.
31. Hopkins, W. D. (2006). Comparative and familial analysis of handedness in great apes. Psychological Bulletin, 132(4), 538-559.
32. Hopkins, W. D. (in press-a). Behavioral and brain asymmetries in chimpanzees: A case for continuity. Annals of the New York Academy of Sciences, 1288, 17-35.
33. Hopkins, W. D. (in press-b). Independence of data points in the measurement of handedness: Statistical problem or urban myth? American Journal of Physical Anthropology, 151(1), 151-157.
34. Hopkins, W. D., & Cantalupo, C. (2004). Handedness in chimpanzees is associated with asymmetries in the primary motor but not with homologous language areas. Behavioral Neuroscience, 118, 1176-1183.
35. Hopkins, W. D., & Cantalupo, C. (2005). Individual and setting differences in the hand preferences of chimpanzees (Pan troglodytes): A critical analysis and some alternative explanations. Laterality, 10, 65-80.
36. Hopkins, W. D., & de Waal, F. B. M. (1995). Behavioral laterality in captive bonobos (Pan paniscus): Replication and extension. International Journal of Primatology, 16, 261-276.
37. Hopkins, W. D., Gardner, M., Mingle, M., Reamer, L., & Schapiro, S. J. (in press). Within- and between-task consistency in hand use as a means of characterizing hand preferences in captive chimpanzees (Pan troglodytes). Journal of Comparative Psychology.
38. Hopkins, W. D., Phillips, K. A., Bania, A., Calcutt, S. E., Gardner, M., Russell, J. L., ... Schapiro, S. J. (2011). Hand preferences for coordinated bimanual actions in 777 great apes: Implications for the evolution of handedness in Hominins. Journal of Human Evolution, 60, 605-611.
39. Hopkins, W. D., Pika, S., Liebal, K., Bania, A., Meguerditchian, A., Gardner, M., & Schapiro, S. J. (2012). Handedness for manual gestures in great apes: A meta-analysis. In S. Pika & K. Liebal (Eds.), Current developments in non-human primate gesture research. Amsterdam: John Benjamins Publishing.
40. Hopkins, W. D., Russell, J., Cantalupo, C., Freeman, H., & Schapiro, S. (2005). Factors influencing the prevalence and handedness for throwing in captive chimpanzees (Pan troglodytes). Journal of Comparative Psychology, 119(4), 363-370.
41. Hopkins, W. D., Russell, J., Hook, M., Braccini, S., & Schapiro, S. (2005). Simple reaching is not so simple: Association between hand use and grip preferences in captive chimpanzees. International Journal of Primatology, 26(2), 259-277.
42. Hopkins, W. D., Russell, J. L., & Cantalupo, C. (2007). Neuroanatomical correlates of handedness for tool use in chimpanzees (Pan troglodytes): Implication for theories on the evolution of language. Psychological Science, 18(11), 971-977.
43. Hopkins, W. D., Russell, J. L., Freeman, H., Buehler, N., Reynolds, E., & Schapiro, S. J. (2005). The distribution and development of handedness for manual gestures in captive chimpanzees (Pan troglodytes). Psychological Science, 16(6), 487-493.
44. Hopkins, W. D., Russell, J. L., Remkus, M., Freeman, H., & Schapiro, S. J. (2007). Handedness and grooming in Pan troglodytes: Comparative analysis between findings in captive and wild chimpanzees. International Journal of Primatology, 28, 1315-1326.
45. Hopkins, W. D., Russell, J. L., Schaeffer, J. A., Gardner, M., & Schapiro, S. J. (2009). Handedness for tool use in captive chimpanzees (Pan troglodytes): Sex differences, performance, heritability and comparion to the wild. Behaviour, 146, 1463-1483.
46. Hopkins, W. D., Taglialatela, J., Leavens, D. A., Russell, J. L., & Schapiro, S. J. (2010). Behavioral and brain asymmetries in chimpanzees. In E. V. Lonsdorf, S. R. Ross, & T. Matsuzawa (Eds.), The mind of the chimpanzee (pp. 60-74). Chicago: University of Chicago Press.
47. Humle, T., & Matsuzawa, T. (2009). Laterality in hand use across four tool use behaviors among the wild chimpanzees of Bossou, Guinea, West Africa. American Journal of Primatology, 71, 40-48.
48. Jones-Engel, L. E., & Bard, K. A. (1996). Precision grips in young chimpanzees. American Journal of Primatology, 39, 1-15.
49. Knecht, S., Drager, B., Deppe, M., Bobe, L., Lohmann, H., Floel, A., ... Henningsen, H. (2000). Handedness and hemispheric language dominance in healthy humans. Brain, 123(12), 2512-2518.
50. LaCreuse, A., Parr, L. A., Smith, H. M., & Hopkins, W. D. (1999). Hand preferences for a haptic task in chimpanzees (Pan troglodytes). International Journal of Primatology, 20(6), 867-881.
51. Lambert, M. (in press). Hand preference for bimanual and unimanual feeding in captive gorillas: Extension in a second colony of apes. American Journal of Physical Anthropology, 641-647.
52. Laurence, A., Wallez, C., & Blois-Heulin, C. (2011). Task complexity, posture, age, sex: which is the main factor influencing manual laterality in captive Cercocebus torquatus torquatus? Laterality, 16(5), 586-606. doi: 10.1080/1357650X.2010.501338
53. Lehman, R. A. W. (1993). Manual preference in prosimians, monkeys, and apes. In J. P. Ward & W. D. Hopkins (Eds.), Primate laterality: Current behavioral evidence of primate asymmetries (pp. 107-124). New York: Springer-Verlag.
54. Lilak, A. L., & Phillips, K. A. (2007). Consistency in hand preference across low-level and high-level tasks in capuchin monkeys (Cebus apella). American Journal of Primatology, 69, 1-12.
55. Llorente, M., Mosquera, M., & Fabre, M. (2009). Manual laterality for simple reaching and bimanual coordinated task in naturalistic housed. Pan troglodytes International Journal of Primatology, 30, 183-197.
56. Llorente, M., Palou, L., Carrasco, L., Riba, D., Mosquera, M., Colell, M., ... Feliu, O. (2010). Population-level right handedness for a coordinated bimanual task in naturalistic housed chimpanzees: Replication and extension in 114 animals from Zambia and Spain. American Journal of Primatology, 71, 1-10.
57. Lonsdorf, E. V., & Hopkins, W. D. (2005). Wild chimpanzees show population level handedness for tool use. Proceedings of the National Academy of Sciences United States of America, 102, 12634-12638.
58. Machlis, L., Dodd, P. W. D., & Fentress, J. C. (1985). The pooling fallacy: Problems arising when individuals contribute more than one observation to the data set. Zeitschrift fur Tierpsychologie, 68(3), 201-214.
59. MacNeilage, P. F., Studdert-Kennedy, M. G., & Lindblom, B. (1987). Primate handedness reconsidered. Behavioral and Brain Sciences, 10, 247-303.
60. Marchant, L. F., & McGrew, W. C. (1991). Laterality of function in apes: A meta-analysis of methods. Journal of Human Evolution, 21, 425-438.
61. Marchant, L. F., & McGrew, W. C. (1996). Laterality of limb function in wild chimpanzees of Gombe National Park: Comprehensive study of spontaneous activities. Journal of Human Evolution, 30, 427-443.
62. Marchant, L. F., & McGrew, W. C. (2007). Ant fishing by wild chimpanzees is not lateralised. Primates, 48, 22-26.
63. Marchant, L. F., McGrew, W. C., & Eibl-Eibesfeldt, I. (1995). In human handedness universal? Ethological analyses from three traditional cultures. Ethology, 101(3), 239-258.
64. Martin, P., & Bateson, P. (1986). Measuring behaviour: An introductory guide. Cambridge: Cambridge University Press.
65. McGrew, W. C., & Marchant, L. F. (1992). Chimpanzees, tools, and termites: Hand preference or handedness? Current Anthropology, 33, 114-119.
66. McGrew, W. C., & Marchant, L. F. (1996). On which side of the apes? In W. C. McGrew, L. F. Marchant, & T. Nishida (Eds.), Great ape societies (pp. 255-272). Cambridge: Cambridge University Press.
67. McGrew, W. C., & Marchant, L. F. (1997). On the other hand: Current issues in and meta-analysis of the behavioral laterality of hand function in non-human primates. Yearbook of Physical Anthropology, 40, 201-232.
68. McGrew, W. C., & Marchant, L. F. (2001). Ethological study of manual laterality in the chimpanzees of the Mahale mountains, Tanzania. Behaviour, 138, 329-358.
69. Meguerditchian, A., Calcutt, S. E., Lonsdorf, E. V., & Ross, S. R. (2010). Captive gorillas are right-handed for bimanual feeding. American Journal of Physical Anthropology, 141, 638-645.
70. Meguerditchian, A., Donnot, J., Molesti, S., Francioly, R., & Vauclair, J. (2012). Sex difference in squirrel monkeys' handedness for unimanual and bimanual tasks. Animal Behaviour, 83, 635-643.
71. Meunier, H., Blois-Heulin, C., & Vauclair, J. (2011). A new tool for measuring hand preference in non-human primates: Adaptation of Bishop's Quantifying Hand Preference task for olive baboons. Behavioural Brain Research, 218, 1-7.
72. Meunier, H., & Vauclair, J. (2007). Hand preferences on unimanual and bimanual tasks in white-face capuchins. American Journal of Primatology, 69, 1064-1069.
73. Meunier, H., Vauclair, J., & Fagard, J. (2012). Human infants and baboons show the same pattern of handedness for a communicative gesture. PLoS ONE, 7(3), e33959.
74. Michel, G. F., Sheu, C. F., & Brumley, M. R. (2002). Hand use preferences from 7 to 11 months of age as revealed by latent class analysis. Developmental Psychobiology, 40, 1-13.
75. Mittra, E. S., Fuentes, A., & McGrew, W. C. (1997). Lack of hand preference in wild hanuman langurs (Presbytis entellus). American Journal of Physical Anthropology, 103, 455-461.
76. Morino, L. (2011). Left-hand rpeference for a complex manual task in a populaiton of wild siamangs (Symphalangus syndactylus). International Journal of Primatology, 32, 793-800.
77. Nishida, T., McGrew, W. C., Marchant, L. F. (in press). Wild chimpanzees at Mahale are not manually lateralised for throwing. Pan Africa News Letter, 19 (2), 1-3.
78. Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97-113.
79. Panger, M. A. (1998). Hand preference in free-ranging white-throated capuchins (Cebus capucinus) in Costa Rica. International Journal of Primatology, 19, 133-163.
80. Papademetriou, E., Sheu, C. F., & Michel, G. F. (2005). A meta-analysis of primate hand preferences for reaching and other hand-use measures. Journal of Comparative Psychology, 119, 33-48.
81. Parnell, R. J. (2001). Hand preference for food processing in wild western lowland gorillas (Gorilla gorilla gorilla). Journal of Comparative Psychology, 115, 365-375.
82. Perelle, I. B., & Ehrman, L. (1994). An international study of human handedness: The data. Behavior Genetics, 24, 217-227.
83. Peters, H. H., & Rogers, L. J. (2007). Limb use and preferences in wild orang-utans during feeding and locomotor behavior. American Journal of Primatology, 69, 1-15.
84. Phillips, K., & Sherwood, C. C. (2005). Primary motor cortex asymmetry correlates with handedness in capuchin monkeys (Cebus apella). Behavioral Neuroscience, 119, 1701-1704.
85. Porac, C., & Coren, S. (1981). Lateral preferences and human behavior. New York: Springer.
86. Rigamonti, M. M., Spiezio, C., Poli, M. D., & Fazio, F. (2005). Laterality of manual fucntion in foraging and positional behavior in wild indri (Indri indri). American Journal of Primatology, 65, 27-38.
87. Rogers, L. J., & Kaplan, G. (1995). Hand preferences and other lateral biases in rehabilitated orangutans, Pongo pygmaeus pygmaeus. Animal Behaviour, 51, 13-25.
88. Salmaso, D., & Longoni, A. M. (1985). Problems in the assessment of handedness. Cortex, 21, 533-549.
89. Schmitt, V., Melchisedech, S., Hammerschmidt, K., & Fischer, J. (2008). Hand preferences in barbary macaques (Macaca sylvanus). Laterality, 13(2), 143-157.
90. Schweitzer, C., Bec, P., & Blois-Heulin, C. (2007). Does the complexity of the task influence laterality in De Brazza's monkeys (Cercopithecus neglectus)? Ethology, 113, 993-994.
91. Smith, H. M., & Thompson, C. L. (2011). Observations of hand preference in wild groups of white-faced sakis (Pithecia pithecia) in Suriname. American Journal of Primatology, 73, 655-664.
92. Spinozzi, G., & Cacchiarelli, B. (2000). 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, 38(13), 1685-1692.
93. Spinozzi, G., Castornina, M. G., & Truppa, V. (1998). Hand preferences for unimanual and coordinated-bimanual tasks in tufted capuchin monkeys (Cebus apella). Journal of Comparative Psychology, 112, 183-191.
94. Spinozzi, G., Truppa, V., & Lagana, T. (2004). Grasping behavior in tufted capuchin monkeys (Cebus apella): Grip types and manual laterality for picking up a small food item. American Journal of Physical Anthropology, 125, 30-41.
95. Sugiyama, Y. (1995). Tool-use for catching ants by chimpanzees at Bossou and Monts Nimba, West Africa. Primates, 36, 193-205.
96. Sugiyama, Y., Fushimi, T., Sakura, O., & Matsuzawa, T. (1993). Hand preference and tool use in wild chimpanzees. Primates, 34, 151-159.
97. Tonooka, R., & Matsuzawa, T. (1995). Hand preferences in captive chimpanzees (Pan troglodytes) in simple reaching for food. International Journal of Primatology, 16, 17-34.
98. Vauclair, J., Meguerditchian, A., & Hopkins, W. D. (2005). Hand preferences for unimanual and coordinated bimanual tasks in baboons (Papio anubis). Cognitive Brain Research, 25, 210-216.
99. Warren, J. M. (1980). Handedness and laterality in humans and other animals. Physiological Psychology, 8, 351-359.
100. Zhao, D., Gao, X., & Li, B. (2010). Hand preference for spontaneously unimanual and bimanual coordinated tasks in wild Sichuan snub-nosed monkeys: Implications for hemispheric specialization. Behavioural Brain Research, 208, 85-89.
101. Zhao, D., Gao, X., Li, B., & Wantanabe, K. (2008). First wild evidence of neonate nipple preference and maternal cradling laterality in Old World monkeys: A preliminary study from Rhinopithecus roxellana. Behavioral Processes, 77(3), 364-368.
102. Zhao, D., Hopkins, W. D., & Li, B. (2012). Handedness in nature: First evidence of manual laterality on bimanual coordinated tube task in wild primates. American Journal of Physical Anthropology, 148, 36-44.