Abstract
In most experimental work on animal cognition, researchers attempt to control for multiple interacting variables by training subjects prior to testing, allowing subjects to participate voluntarily, and providing subjects with food rewards. However, do such methods encourage selection bias from subjects’ personalities? In this study, we trained eighteen zoo-housed capuchin monkeys (Sapajus apella) for two experiments, under conditions of positive reinforcement (i.e. food rewards) and free-choice participation. Using a combination of behavioral and rater-based methods, we identified and validated five personality dimensions in these capuchins (Assertiveness, Openness, Neuroticism, Sociability, and Attentiveness). Scores on Openness were positively related to individual differences in monkey task participation, reflecting previous work showing that such individuals are often more active, curious, and willing to engage in testing. We also found a negative relationship between scores on Assertiveness and performance on tasks, which may reflect the trade-offs between speed and accuracy in these animals’ decision-making. Highly Assertive individuals (the most sociable within monkey groups) may also prioritize social interactions over engaging in research. Lastly, monkeys that consistently participated and performed well on both tasks showed significantly higher Openness and lower Assertiveness compared to others, mirroring relationships found between personality, participation, and performance among all participants. Participation and performance during training was clearly biased toward individuals with particular personalities (i.e. high Openness, low Assertiveness). Results are discussed in light of the need for careful interpretation of comparative data on animal cognition and the need for researchers to take personality selection bias more seriously.
Similar content being viewed by others
References
ASAB (2012) Guidelines for the treatment of animals in behavioural research and teaching. Anim Behav 83:301–309
Bacon ES (1980) Curiosity in the American black bear. Bears: their biology and management, vol. 4, a selection of papers from the fourth international conference on bear research and management, Kalispell, Montana, USA, February 1977, pp 153–157
Bates TC, Shieles A (2003) Crystallized intelligence as a product of speed and drive for experience: the relationship of inspection time and openness to g and Gc. Intelligence 31:275–287
Benson-Amram S, Holekamp KE (2012) Innovative problem solving by wild spotted hyenas. Proc R Soc B-Biol Sci. doi:10.1098/rspb.2012.1450
Bergman TJ, Kitchen DM (2009) Comparing responses to novel objects in wild baboons (Papio ursinus) and geladas (Theropithecus gelada). Anim Cogn 12:63–73
Biondi LM, Bo MS, Vassallo AI (2010) Inter-individual and age differences in exploration, neophobia and problem-solving ability in a neotropical raptor (Milvago chimango). Anim Cogn 13:701–710. doi:10.1007/s10071-010-0319-8
Biro PA, Dingemanse NJ (2009) Sampling bias resulting from animal personality. Trends Ecol Evol 24:66–68. doi:10.1016/j.tree.2008.11.001
Blaney PH, Millon T (2009) Oxford textbook of psychopathology. Oxford University Press, Oxford
Boogert NJ, Reader SM, Laland KN (2006) The relation between social rank, neophobia and individual learning in starlings. Anim Behav 72:1229–1239
Bornehag CG, Sundell J, Sigsgaard T, Janson S (2004) Potential self- selection bias in a nested case-control study on indoor environmental factors and their association with asthma and allergic symptoms among pre-school children. Scand J Public Health 34(5):534–543
Burns JG, Rodd FH (2008) Hastiness, brain size and predation regime affect the performance of wild guppies in a spatial memory task. Anim Behav 76:911–922. doi:10.1016/j.anbehav.2008.02.017
Bussey TJ, Padain TL, Skillings EA, Winters BD, Morton AJ, Saksida LM (2008) The touchscreen cognitive testing method for rodents: how to get the best out of your rat. Learn Memory 15:516–523. doi:10.1101/lm.987808
Cahan S, Gamliel E (2006) Definition and measurement of selection bias: from constant ratio to constant difference. J Edu Meas 43:131–144
Campbell AM, Davalos DB, McCabe DP, Troup LJ (2011) Executive functions and extraversion. Pers Individ Dif 51:720–725
Carere C, Locurto C (2011) Interaction between animal personality and animal cognition. Curr Zool 57:491–498
Clark FE (2011) Great ape cognition and captive care: can cognitive challenges enhance well-being? Appl Anim Behav Sci 135:1–12. doi:10.1016/j.applanim.2011.10.010
Dawkins R, Carlisle TR (1976) Parental investment, mate desertion, and a fallacy. Nature 262:131–133
Deaner R, van Schaik C, Johnson V (2006) Do some taxa have better domain-general cognition than others? A meta-analysis of nonhuman primate studies. Evol Psychol 4:149–196
Evans TA, Beran MJ, Chan B, Klein ED, Menzel CR (2008) An efficient computerized testing method for the capuchin monkey (Cebus apella): adaptation of the LRC-CTS to a socially housed nonhuman primate species. Behav Res Methods 40:590–596. doi:10.3758/BRM.40.2.590
Fagot J, Paleressompoulle D (2009) Automatic testing of cognitive performance in baboons maintained in social groups. Behav Res Methods 41:396–404. doi:10.3758/BRM.41.2.396
Fragaszy DM, Visalberghi E, Fedigan LM (2004) The complete capuchin: the biology of the genus Cebus. Cambridge University Press, New York
Garamszegi LZ, Eens M, Török J (2009) Behavioural syndromes and trappability in free-living collared flycatchers, Ficedula albicollis. Anim Behav 77:803–812. doi:10.1016/j.anbehav.2008.12.012
Garber PA, Gomes DF, Bicca-Marques JC (2012) Experimental field study of problem-solving using tools in free-ranging capuchins (Sapajus nigritus, formerly Cebus nigritus). Am J Primatol 74:344–358. doi:10.1002/ajp.20957
Gosling SD, John OP (1999) Personality dimensions in nonhuman animals: a cross-species review. Curr Dir Psychol Sci 8:69–75
Herrelko ES, Vick S-J, Buchanan-Smith HM (2012) Cognitive research in zoo-housed chimpanzees: influence of personality and impact on welfare. Am J Primatol. doi:10.1002/ajp.22036
Kashdan TB, Rose P, Fincham FD (2004) Curiosity and exploration: facilitating positive subjective experiences and personal growth opportunities. J Pers Assess 82:291–305
Leonardi R, Buchanan-Smith HM, Dufour V, MacDonald C, Whiten A (2010) Living together: behavior and welfare in single and mixed species groups of capuchin (Cebus apella) and squirrel monkeys (Saimiri sciureus). Am J Primatol 72:33–47
MacDonald C, Whiten A (2011) The ‘Living Links to Human Evolution’ Research Centre in Edinburgh Zoo: a new endeavour in collaboration. Int Zoo Yearbook 45:1–17. doi:10.111/j.1748-1090.2010.00120.x
Malani A (2008) Patient enrollment in medical trials: selection bias in a randomized experiment. J Econom 144:341–351
Morton FB, Lee PC, Buchanan-Smith HM, Brosnan S, Thierry B, Paukner A, de Waal FBM, Widness J, Essler J, Weiss A (2013) Personality structure in brown capuchin monkeys: comparisons with chimpanzees, orangutans, and rhesus macaques. J Comp Psychol. doi:10.1037/a0031723
Rehbein L, Moss MB (2002) Explorations of three modes of spatial cognition in the monkey. Psicológica 23:139–163
Reid GMcG, Macdonald AA, Fidgett AL, Hiddinga B, Leus K (2008) Developing the research potential of zoos and aquaria. The EAZA research strategy EAZA executive office, Amsterdam. ISBN: 978-90-77879-10-8
Sih A, Del Giudice M (2012) Linking behavioural syndromes and cognition: a behavioural ecology perspective. Phil Trans R Sci B. doi:10.1098/rstb.2012.0216
Watson SL, Ward JP (1996) Temperament and problem solving in the small- eared bushbaby (Otolemur garnettii). J Comp Psychol 110:377–385
Weiss A, Inoue-Murayama M, Hong K-W et al (2009) Assessing chimpanzee personality and subjective well-being in Japan. Am J Primatol 71:283–292. doi:10.1002/ajp.v71:4
Weiss A, Adams MJ, Widdig A, Gerald MS (2011) Rhesus macaques (Macaca mulatta) as living fossils of hominoid personality and subjective well-being. J Comp Psychol 125:72–83. doi:10.1037/a0021187
Wilson ADM, Thomas RB, Keegan PM, Cooke SJ, Godin J-GJ (2011) Capture technique and fish personality: angling targets timid bluegill sunfish, Lepomis macrochirus. Can J Fish Aquat Sci 68:749–757. doi:10.1139/F2011-019
Acknowledgments
This research would not have been possible without the many people involved in the capuchin personality study, particularly A. Weiss, S. Brosnan, and B. Thierry. F.B.M. would also like to personally thank Prof. Andrew Whiten, Director of Living Links (RZSS), who gave permission to conduct research there, and all of the Living Links/RZSS staff and students who kindly provided support and assistance. We also thank K. Howie who gave helpful statistical advice, P. Hancock who kindly conducted the bootstrapping analysis used in this study, the BERG (University of Stirling) for their feedback, and J. Anderson, S. Brosnan, and the anonymous reviewers for providing useful comments on earlier drafts. F.B.M gratefully acknowledges the Charles A. Lockwood Memorial Fund and the University of Stirling for funding. The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Morton, F.B., Lee, P.C. & Buchanan-Smith, H.M. Taking personality selection bias seriously in animal cognition research: a case study in capuchin monkeys (Sapajus apella). Anim Cogn 16, 677–684 (2013). https://doi.org/10.1007/s10071-013-0603-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-013-0603-5