Humans exhibit population level handedness for the right hand; however, the evolution of this behavioral phenotype is poorly understood. Here, we compared the laterality of a simple task (grooming) and a complex task (tool use) to investigate whether increasing task difficulty elicited individual hand preference among a group of captive bonobos (Pan paniscus). Subjects were 17 bonobos housed at the Columbus Zoo and Aquarium. Laterality of grooming was recorded using group scans; tool use was recorded using all-occurrence sampling. Grooming was characterized as unimanual or bimanual, and both tasks were scored as right-handed or left-handed. Most individuals did not exhibit significant hand preference for unimanual or bimanual (asymmetrical hand use) grooming, although 1 individual was lateralized for each. For the 8 subjects who engaged in termite fishing enough for statistical testing, 7 individuals exhibited significant laterality and strong individual hand preference. Four subjects preferred their left hand, 3 preferred their right, and 1 had no preference. Grooming, a simple behavior, was not lateralized in this group, yet a more complex behavior revealed a strong individual hand preference, and these results are congruent with other recent findings that demonstrate complex tasks elicit hand preference in bonobos.

Keywords:
Grooming, Tool use, Termite fishing, Laterality, Hand preference, Bonobo, Pan paniscus
1.
Altmann J (1974). Observational study of behavior: sampling methods. Behaviour 49: 227-267.
2.
Annett M (2002). Handedness and Brain Asymmetry: The Right Shift Theory. Hove, Psychology Press.
3.
Bardo A, Pouydebat E, Meunier H (2015). Do bimanual coordination, tool use, and body posture contribute equally to hand preferences in bonobos? Journal of Human Evolution 82: 159-169.
4.
Boesch C (1991). Handedness in wild chimpanzees. International Journal of Primatology 12: 541-558.
5.
Bogart SL, Pruetz JD, Ormiston LK, Russell JL, Meguerditchian A, Hopkins WD (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.
6.
Boose KJ, White FJ, Meinelt A (2013). Sex differences in tool use acquisition in bonobos (Pan paniscus). American Journal of Primatology 75: 917-926.
7.
Brand CM, Marchant LF (2015). Hair plucking in captive bonobos (Pan paniscus). Applied Animal Behaviour Science 171: 192-196.
8.
Byrne RW (2016). Evolving Insight. Oxford, Oxford University Press.
9.
Byrne RW, Byrne JM (1991). Hand preferences in the skilled gathering tasks of mountain gorillas (Gorilla g. berengei). Cortex 27: 521-546.
10.
Calvin WH (1983). A stone's throw and its launch window: timing precision and its implication for language and hominids brain. Journal of Theoretical Biology 104: 121-135.
11.
Cashmore L (2009). Can hominin “handedness” be accurately assessed? Annals of Human Biology 36: 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.
Cavanagh T, Berbesque JC, Wood B, Marlowe F (2016). Hadza handedness: lateralized behaviors in a contemporary hunter-gatherer population. Evolution and Human Behavior 37: 202-209.
14.
Chapelain AS, Hogervost E, Mbonzo P, Hopkins WD (2011). Hand preferences for bimanual coordination in 77 bonobos (Pan paniscus): replication and extension. International Journal of Primatology 32: 491-510.
15.
Corballis MC (2003). From mouth to hand: gesture, speech and the evolution of right-handedness. Behavioral and Brain Sciences 26: 199-260.
16.
Corp N, Byrne RW (2004). Sex differences in chimpanzee handedness. American Journal of Physical Anthropology 123: 62-68.
17.
Estalrrich A, Rosas A (2013). Handedness in Neanderthals from El Sidrón (Asturias, Spain): evidence from instrumental striations with ontogenetic inferences. PLoS One 8: e62797.
18.
Fagot J, Vauclair J (1991). Manual laterality in nonhuman primates: a distinction between handedness and manual specialization. Psychological Bulletin 109: 76-89.
19.
Fiore I, Bondioli L, Radovčić J, Frayer DW (2015). Handedness in the Krapina Neanderthals: a re-evaluation. Paleo Anthropology 2015: 19-36.
20.
Frayer DW, Clarke RJ, Fiore I, Blumenschine RJ, Pérez-Pérez A, Martinez LM, Estebaranz F, Holloway R, Bondioli L (2016). OH-65: The earliest evidence for right-handedness in the fossil record. Journal of Human Evolution 100: 65-72.
21.
Furuichi T, Sanz C, Koops K, Sakamaki T, Ryu H, Tokuyama N, Morgan D (2015). Why do wild bonobos not use tools like chimpanzees? Behaviour 152: 425-460.
22.
Geschwind N, Galaburda AM (1985). Cerebral lateralization. Biological mechanisms, associations and pathology: a hypothesis and a program for research. Archives of Neurology 42: 428-654.
23.
Gruber T, Clay Z, Zuberbühler K (2010) A comparison of bonobo and chimpanzee tool use: evidence for a female bias in the Pan lineage. Animal Behaviour 80: 1023-1033.
24.
Harrison RM, Nystrom P (2008). Handedness in captive bonobos (Pan paniscus). Folia Primatologica 79: 253-268.
25.
Hopkins WD (1995). Hand preferences for a coordinated bimanual task in 110 chimpanzees (Pan troglodytes): cross-sectional analysis. Journal of Comparative Psychology 109: 291-297.
26.
Hopkins WD (1999). On the other hand: statistical issues in the assessment and interpretation of hand preference data in nonhuman primates. International Journal of Primatology 20: 851-866.
27.
Hopkins WD (2006). Comparative and familial analysis of handedness in great apes. Psychological Bulletin 132: 538-559.
28.
Hopkins WD, 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.
29.
Hopkins WD, Phillips KA, Bania A, Calcutt SE, Gardner M, Russell J, Schaeffer J, Lonsdorf EV, Ross SR, Schapiro SJ (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.
30.
Hopkins WD, Russell JL, Remkus M, Freeman H, Shapiro SJ (2007). Handedness and grooming in Pan troglodytes: comparative analysis between findings in captive and wild individuals. International Journal of Primatology 28: 1315-1326.
31.
Hopkins WD, Schaeffer J, Russell JL, Bogart SL, Meguerditchian A, Coulon O (2015). A comparative assessment of handedness and its potential neuroanatomical correlates in chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). Behaviour 152: 461-492.
32.
Humle T, Matsuzawa T (2009). Laterality in hand use across four tool-use behaviours among the wild chimpanzees of Bossou, Guinea, West Africa. American Journal of Primatology 71: 40-48.
33.
Ingmanson EJ (1998). Right and left hand use preferences in a power grip task among Pan paniscus at Wamba, Zaire. American Journal of Physical Anthropology 26: 125.
34.
Ingmanson EJ (2005). Hand-use preferences among Pan paniscus (bonobos) at Wamba, Democratic Republic of Congo. American Journal of Primatology 66: 69-70.
35.
Kano T (1992). The Last Ape: Pygmy Chimpanzee Behavior and Ecology. Stanford, Stanford University Press.
36.
Kimura D (1979). Neuromotor mechanisms in the evolution of human communication. In Neurobiology of Social Communication in Primates: An Evolutionary Perspective (Steklis HD, Raleigh MJ, eds.), pp 197-220. New York, Academic Press.
37.
Koops K, Furuichi T, Hashimoto C (2015). Chimpanzees and bonobos differ in intrinsic motivation for tool use. Scientific Reports 5: 11356.
38.
Leca JB, Gunst N, Huffman M (2011). Complexity in object manipulation by Japanese macaques (Macaca fuscata): a cross-sectional analysis of manual coordination in stone handling patterns. Journal of Comparative Psychology 125: 61-71.
39.
Lilak AL, Phillips KA (2008). Consistency of hand preference across low-level and high-level tasks in capuchin monkeys (Cebus apella). American Journal of Primatology 70: 254-260.
40.
Lonsdorf EV, Hopkins WD (2005). Wild chimpanzees show population-level handedness for tool use. Proceedings of the National Academy of Sciences 102: 12634-12638.
41.
Marchant LF (2015). Laterality of hand function. In Mahale Chimpanzees: 50 Years of Research (Nakamura M, Hosaka K, Itoh N, Zamma K, eds.), pp 556-567. Cambridge, Cambridge University Press.
42.
Marchant LF, McGrew WC (1994). An ethological perspective on human handedness. In The Ethological Roots of Culture (Gardner RA, Chiarelli B, Plooij FC, eds.), pp 375-384. New York, Springer.
43.
Marchant LF, McGrew WC (1996). Laterality of limb function in wild chimpanzees of Gombe National Park: comprehensive study of spontaneous activities. Journal of Human Evolution 30: 427-443.
44.
Marchant LF, McGrew WC (2013). Handedness is more than laterality: lessons from chimpanzees. In The Evolution of Human Handedness (McGrew WC, Marchant LF, Schiefenhövel W, eds.). Annals of the New York Academy of Sciences 1288: 1-8.
45.
Marchant LF, McGrew WC, Eibl-Eisbesfeldt I (1995). Is human handedness universal? Ethological analyses from three traditional societies. Ethology 101: 239-258.
46.
McGrew WC, Marchant LF (1992). Chimpanzees, tools, and termites: hand preference or handedness? Current Anthropology 33: 114-119.
47.
McGrew WC, Marchant LF (1996). On which side of the apes? Ethological study of laterality of hand use. In Great Ape Societies (McGrew WC, Marchant LF, Nishida T, eds.), pp 255-271. Cambridge, Cambridge University Press.
48.
McGrew WC, Marchant LF (1997). On the other hand: current issues in and meta-analysis of the behavioral laterality of hand function in nonhuman primates. Yearbook of Physical Anthropology 40: 201-232.
49.
McGrew WC, Marchant LF (2001). Ethological study on manual laterality in the chimpanzees of the Mahale Mountains, Tanzania. Behaviour 138: 329-358.
50.
McKenna JJ (1978). Biosocial functions of grooming behavior among the common Indian langur monkey (Presbytis entellus). American Journal of Physical Anthropology 48: 503-509.
51.
McNeilage PF, Studdert-Kennedy MG, Lindblom B (1987). Primate handedness reconsidered. Behavioral and Brain Sciences 10: 247-303.
52.
Neufuss J, Humle T, Cremaschi A, Kivell TA (2017). Nut-cracking behaviour in wild-born, rehabilitated bonobos (Pan paniscus): a comprehensive study of hand-preference, hand grips and efficiency. American Journal of Primatology 79: 1-16.
53.
Papademetriou E, Sheu CF, Michel GF (2005). A meta-analysis of primate hand preferences, particularly for reaching. Journal of Comparative Psychology 119: 33-48.
54.
Sanz CM, Morgan DB, Hopkins WD (2016). Lateralization and performance asymmetries in the termite fishing of wild chimpanzees in the Goualougo Triangle, Republic of Congo. American Journal of Primatology 78: 1190-1200.
55.
Shafer DD (1997). Hand preference behaviors shared by two groups of captive bonobos. Primates 38: 303-313.
56.
Sokal RR, Rohlf FJ (2011). Biometry. New York, Freeman.
57.
Uomini NT (2009). The prehistory of handedness: archaeological data and comparative ethology. Journal of Human Evolution 57: 411-419.
58.
Vauclair J (2004). Lateralization of communicative signals in nonhuman primates and the hypothesis of the gestural origin of language. Interaction Studies 5: 365-386.
59.
Volpato V, Macchiarelli R, Guatelli-Steinberg D, Fiore I, Bondioli L, Frayer DW (2012). Hand to mouth in a Neandertal: right-handedness in Regourdou 1. PLoS One 7: e43949.
60.
White FJ, Waller MT, Cobden AK, Malone NM (2008). Lomako bonobo population dynamics, habitat productivity, and the question of tool use. American Journal of Physical Anthropology 46: 222.
61.
Whiten A, Goodall J, McGew WC, Nishida T, Reynolds V, Sugiyama Y, Tutin CEG, Wrangham RW, Boesch C (1999). Cultures in chimpanzees. Nature 399: 682-685.
62.
Zhao DP, Gao X, Li BG (2010). Hand preference for spontaneously unimanual and bimanual coordinated tasks in wild Sichuan snub-nosed monkeys: implication for hemispheric specialization. Behavioral Brain Research 208: 85-89.
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