Abstract
Twenty-eight captive Sichuan snub-nosed monkeys (Rhinopithecus roxellana) were involved in the current study. Many individuals showed handedness, with a modest tendency toward left-hand use especially for animate targets, although no group-level handedness was found. There was no significant gender difference in the direction and strength of hand preference for both targets. Females showed a significantly higher overall rate of actions toward animate targets than inanimate targets for both hands, whereas males displayed almost the reversed pattern. There were no significant interactions between lateral hand use and target animacy for either males or females. Most individuals showed rightward or leftward laterality shift trends between inanimate and animate targets. These findings to some extent support the existence of a potential trend concerning a categorical neural distinction between targets demanding functional manipulation (inanimate objects) and those demanding social manipulation (animate objects), even though specialized hand preference based on target animacy has not been fully established in this arboreal Old World monkey species.
Similar content being viewed by others
References
Barnard S, Matthews L, Messori S, Podaliri-Vulpiani M, Ferri N (2016) Laterality as an indicator of emotional stress in ewes and lambs during a separation test. Anim Cogn 19:207–214
Borod JC, Cicero BA, Obler LK, Welkowitz J, Erhan HM, Santschi C, Grunwald IS, Agosti RM, Whalen JR (1998) Right hemisphere emotional perception: evidence across multiple channels. Neuropsychology 12:446–458
Casperd JM, Dunbar RIM (1996) Asymmetries in the visual processing of emotional cues during agonistic interactions by gelada baboons. Behav Process 37:57–65
Chen FG, Min ZL, Lou SY, Xie WZ (1983) An observation on the behavior and some ecological habits of the Sichuan snub-nosed monkeys (Rhinopitheus roxellana) in Qinling Mountains. Acta Theriol Sinica 3:141–146
Corballis MC (2002) From hand to mouth: the origins of language. Princeton University Press, Princeton
Davidson RJ (1995) Cerebral asymmetry, emotion, and affective style. In: Davidson RJ, Hugdahl K (eds) Brain asymmetry. MIT Press, Cambridge, pp 361–387
Demaree HA, Everhart DE, Youngstrom EA, Harrison DW (2005) Brain lateralization of emotional processing: historical roots and a future incorporating “dominance”. Behav Cogn Neurosci Rev 4:3–20
Elango N, Lee J, Peng ZG, Loh YHE, Yi SV (2009) Evolutionary rate variation in Old World monkeys. Biol Lett 5:405–408
Fagot J, Vauclair J (1991) Manual laterality in nonhuman primates: a distinction between handedness and manual specialization. Psychol Bull 109:76–89
Forrester GS, Leavens DA, Quaresmini C, Vallortigara G (2011) Target animacy influences gorilla handedness. Anim Cogn 14:903–907
Forrester GS, Quaresmini C, Leavens DA, Spiezio C, Vallortigara G (2012) Target animacy influences chimpanzee handedness. Anim Cogn 15:1121–1127
Forrester GS, Quaresmini C, Leavens DA, Mareschal D, Thomas MSC (2013) Human handedness: an inherited evolutionary trait. Behav Brain Res 237:200–206
Forrester GS, Crawley M, Palmer C (2014) Social environment elicits lateralized navigational paths in two populations of typically developing children. Brain Cogn 91:21–27
Giljov A, Karenina K, Ingram J, Malashichew Y (2015) Parallel emergence of true handedness in the evolution of marsupials and placentals. Curr Biol 25:1878–1884
Greenfield PM (1991) Language, tools, and brain: the ontogeny and phylogeny of hierarchically organized sequential behavior. Behav Brain Sci 14:531–550
Hauser MD (1993) Right hemisphere dominance for the production of facial expression in monkeys. Science 261:475–477
Hook-Costigan MA, Rogers LJ (1998) Lateralized use of the mouth in production of vocalizations by marmosets. Neuropsychologia 36:1265–1273
Hopkins WD (1999) On the other hand: statistical issues in the assessment and interpretation of hand preference data in nonhuman primates. Int J Primatol 20:851–866
Hopkins WD (2007) The evolution of hemispheric specialization in primates. Academic Press, San Diego
Hopkins WD (2013) Independence of data points in the measurement of hand preferences in primates: statistical problem or urban myth? Am J Phys Anthropol 151:151–157
Hopkins WD, Cantalupo C, Wesley MJ, Hostetter AB, Pilcher DL (2002) Grip morphology and hand use in chimpanzees (Pan troglodytes): evidence of a left hemisphere specialization in motor skill. J Exp Psychol 131:412–423
Jones LV, Fiske DW (1953) Models for testing significance of combined results. Psychol Bull 50:375–382
Leliveld LMC, Langbein J, Puppe B (2013) The emergence of emotional lateralization: evidence in non-human vertebrates and implications for farm animals. Appl Anim Behav Sci 145:1–14
Levy J (1977) The mammalian brain and the adaptive advantage of cerebral asymmetry. Ann NY Acad Sci 299:264–272
Liang B, Zhang SY (1998) Hand preference in Sichuan golden monkeys (Rhinopithecus roxellana). Acta Theriol Sinica 18:107–111
Lindell AK (2013) Continuities in emotion lateralization in human and non-human primates. Front Hum Neurosci 7:464
Ma YY, Tian YF, Deng ZY (1988) The hand preference of Presbytis (PR), Rhinopithecus (RH) and Hylobates (HY) in picking up food. Acta Anthropol Sinica 7:177–181
MacNeilage PF (1991) The “postural origin” theory of primate neurobiological asymmetries. In: Krasnegor NA, Rumbaugh DM, Schieflbusch RL (eds) Biological and behavioral determinants of language development. Lawrence Erlbaum Associates, New Jersey, pp 165–188
MacNeilage PF (2007) Present status of the postural origins theory. In: Hopkins WD (ed) The evolution of hemispheric specialization in primates. Academic Press, San Diego, pp 59–91
MacNeilage PF, Studdert-Kennedy MG, Lindblom B (1987) Primate handedness reconsidered. Behav Brain Sci 10:247–303
MacNeilage PF, Rogers LJ, Vallortigara G (2009) Origins of the left and right brain. Sci Am 301:60–67
Porac C, Coren S (1981) Lateral preferences and human behavior. Springer, New York
Quaresmini C, Forrester GS, Spiezio C, Leavens DA, Vallortigara G (2014) Social environment elicits lateralized behaviors in gorillas (Gorilla gorilla gorilla) and chimpanzees (Pan troglodytes). J Comp Psychol 128:276–284
Robins A, Rogers LJ (2006) Lateralized visual and motor responses in the green tree frog, Litoria caerulea. Anim Behav 72:843–852
Rogers LJ (2014) Asymmetry of brain and behavior in animals: its development, function, and human relevance. Genesis 52:S555–S571
Rogers L, Vallortigara G, Andrew RJ (2013) Divided brains: the biology and behaviour of brain asymmetries. Cambridge University Press, New York
Rosa Salva O, Regolin L, Mascalzoni E, Vallortigara G (2012) Cerebral and behavioural asymmetry in animal social recognition. Comp Cogn Behav Rev 7:110–138
Rutherford HJV, Lindell AK (2011) Thriving and surviving: approach and avoidance motivation and lateralization. Emot Rev 3:333–343
Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–589
Wallez C, Vauclair J (2013) Human (Homo sapiens) and baboon (Papio papio) chimeric face processing: right-hemisphere involvement. J Comp Psychol 127:237–244
Zhang P, Li BG, MacIntosh AJJ, Watanabe K (2012) A proximity-based social network of a group of Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Int J Primatol 33:1081–1095
Zhao DP, Li BG (2009) Do deposed adult male Sichuan snub-nosed monkeys (Rhinopithecus roxellana) roam as solitary bachelors or continue to interact with former band members? Curr Zool 55:235–237
Zhao DP, Li BG (2013) Footedness from a spontaneously bipedal posture of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains. Acta Theriol Sinica 33:1–6
Zhao DP, Li BG, Grove CP, Watanabe K (2008a) Impact of male takeover on intra-unit sexual interactions and subsequent interbirth interval of wild Rhinopithecus roxellana. Folia Primatol 79:93–102
Zhao DP, Ji WH, Li BG, Watanabe K (2008b) Mate competition and reproductive correlates of female dispersal in a polygynous primate species (Rhinopithecus roxellana). Behav Process 79:165–170
Zhao DP, Ji WH, Watanabe K, Li BG (2008c) Hand preference during unimanual and bimanual reaching actions in Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Am J Primatol 70:500–504
Zhao DP, Li BG, Watanabe K (2008d) First evidence on foot preference during locomotion in Old World monkeys: a study of quadrupedal and bipedal actions in Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Primates 49:260–264
Zhao DP, Gao X, Li BG, Watanabe K (2008e) First wild evidence of neonate nipple preference and maternal cradling laterality in Old World monkeys: a preliminary study from Rhinopithecus roxellana. Behav Process 77:364–368
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. Behav Brain Res 208:85–89
Zhao DP, Li BG, Watanabe K (2011) Impact of group size on female reproductive success of free-ranging Rhinopithecus roxellana in the Qinling Mountains, China. Folia Primatol 82:1–12
Zhao DP, Hopkins WD, Li BG (2012) Handedness in nature: first evidence of manual laterality on bimanual coordinated tube task in wild primates. Am J Phys Anthropol 148:36–44
Zhao DP, Wang Y, Han KJ, Zhang HB, Li BG (2015) Does target animacy influence manual laterality of monkeys? first answer from northern pig-tailed macaques (Macaca leonina). Anim Cogn 18:931–936
Acknowledgments
We appreciate animal keepers of Beijing Wildlife Zoo for their assistance during data collection.
Funding
This study was funded by National Natural Science Fund of China (No. 31200293), Talent Introduction Fund of Tianjin Normal University of China (No. 5RL115), and “More Than One Thousand Talents Introduction within Three Years” Fund of Tianjin City of China (No. 5KQM110002).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international and Chinese guidelines for the care and use of animals were followed. The research procedure was approved by the academic committee at college of life sciences, Tianjin Normal University of China.
Rights and permissions
About this article
Cite this article
Zhao, D., Tian, X., Liu, X. et al. Effect of target animacy on hand preference in Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Anim Cogn 19, 977–985 (2016). https://doi.org/10.1007/s10071-016-1002-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-016-1002-5