Establishing an infrastructure for collaboration in primate cognition research

Autoři: Drew M. Altschul aff001;  Michael J. Beran aff002;  Manuel Bohn aff003;  Josep Call aff005;  Sarah DeTroy aff004;  Shona J. Duguid aff006;  Crystal L. Egelkamp aff007;  Claudia Fichtel aff008;  Julia Fischer aff008;  Molly Flessert aff002;  Daniel Hanus aff009;  Daniel B. M. Haun aff004;  Lou M. Haux aff010;  R. Adriana Hernandez-Aguilar aff011;  Esther Herrmann aff009;  Lydia M. Hopper aff007;  Marine Joly aff013;  Fumihiro Kano aff014;  Stefanie Keupp aff008;  Alicia P. Melis aff006;  Alba Motes Rodrigo aff015;  Stephen R. Ross aff007;  Alejandro Sánchez-Amaro aff009;  Yutaro Sato aff014;  Vanessa Schmitt aff017;  Manon K. Schweinfurth aff005;  Amanda M. Seed aff005;  Derry Taylor aff013;  Christoph J. Völter aff005;  Elizabeth Warren aff005;  Julia Watzek aff002
Působiště autorů: The University of Edinburgh, Edinburgh, United Kingdom aff001;  Georgia State University, Atlanta, Georgia, United States of America aff002;  Stanford University, Stanford, California, United States of America aff003;  Leipzig University, Leipzig, Germany aff004;  University of St Andrews, St Andrews, United Kingdom aff005;  Warwick Business School, University of Warwick, Coventry, United Kingdom aff006;  Lincoln Park Zoo, Chicago, Illinois, United States of America aff007;  German Primate Center and Leibniz ScienceCampus Primate Cognition, Göttingen, Germany aff008;  Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany aff009;  Center for Adaptive Rationality, Max Planck Institute for Human Development, Berlin, Germany aff010;  Centre for Ecological and Evolutionary Synthesis, University of Oslo, Oslo, Norway aff011;  Department of Social Psychology and Quantitative Psychology, University of Barcelona, Barcelona, Spain aff012;  University of Portsmouth, Portsmouth, United Kingdom aff013;  Kyoto University, Kyoto, Japan aff014;  University of Tübigen, Tübingen, Germany aff015;  University of California San Diego, San Diego, California, United States of America aff016;  Heidelberg Zoo & University of Heidelberg, Heidelberg, Germany aff017;  Messerli Research Institute, University of Veterinary Medicine Vienna, Medical University of Vienna, University of Vienna, Vienna, Austria aff018
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


Inferring the evolutionary history of cognitive abilities requires large and diverse samples. However, such samples are often beyond the reach of individual researchers or institutions, and studies are often limited to small numbers of species. Consequently, methodological and site-specific-differences across studies can limit comparisons between species. Here we introduce the ManyPrimates project, which addresses these challenges by providing a large-scale collaborative framework for comparative studies in primate cognition. To demonstrate the viability of the project we conducted a case study of short-term memory. In this initial study, we were able to include 176 individuals from 12 primate species housed at 11 sites across Africa, Asia, North America and Europe. All subjects were tested in a delayed-response task using consistent methodology across sites. Individuals could access food rewards by remembering the position of the hidden reward after a 0, 15, or 30-second delay. Overall, individuals performed better with shorter delays, as predicted by previous studies. Phylogenetic analysis revealed a strong phylogenetic signal for short-term memory. Although, with only 12 species, the validity of this analysis is limited, our initial results demonstrate the feasibility of a large, collaborative open-science project. We present the ManyPrimates project as an exciting opportunity to address open questions in primate cognition and behaviour with large, diverse datasets.

Klíčová slova:

Animal performance – Animal phylogenetics – Apes – Phylogenetic analysis – Primates – Psychology – Short term memory – Animal cognition


1. Martins EP. Phylogenies and the comparative method in animal behavior. Oxford: Oxford University Press; 1995.

2. Beach FA. The snark was a boojum. Am Psychol. 1950;5: 115–124. doi: 10.1186/1742-9994-12-S1-S20 26816519

3. Hodos W, Campbell CBG. Scala naturae: why there is no theory in comparative psychology. Psychol Rev. 1969;76: 334–350.

4. Lockard RB. Reflections on the fall of comparative psychology: is there a message for us all? Am Psychol. 1971;26: 168–179. doi: 10.1037/h0030816

5. Kappeler PM, Pereira ME. Primate life histories and socioecology. Chicago: University of Chicago Press; 2003.

6. Stevens JR. Replicability and reproducibility in comparative psychology. Front Psychol. 2017;8: 862. doi: 10.3389/fpsyg.2017.00862 28603511

7. Hopper LM. Cognitive research in zoos. Curr Opin Behav Sci. 2017;16: 100–110. doi: 10.1016/j.cobeha.2017.04.006

8. Matsuzawa T. Field experiments on use of stone tools by chimpanzees in the wild. In: Wrangham RW, McGrew WC, de Waal FBM, Heltne PG, editors. In Chimpanzee cultures. Cambridge: MA: Harvard University Press in coop. with The Chicago Academy of Science; 1994. pp. 351–370.

9. Boesch C. What makes us human (Homo sapiens)? The challenge of cognitive cross-species comparison. J Comp Psychol. 2007;121: 227–240. doi: 10.1037/0735-7036.121.3.227 17696649

10. Völter CJ, Tinklenberg B, Call J, Seed AM. Comparative psychometrics: establishing what differs is central to understanding what evolves. Philos Trans R Soc B Biol Sci. 2018;373: 20170283. doi: 10.1098/rstb.2017.0283 30104428

11. MacLean EL, Hare B, Nunn CL, Addessi E, Amici F, Anderson RC, et al. The evolution of self-control. Proc Natl Acad Sci. 2014;111: 2140–2148.

12. Joly M, Micheletta J, De Marco A, Langermans JA, Sterck EHM, Waller BM. Comparing physical and social cognitive skills in macaque species with different. Proc R Soc B Biol Sci. 2017;284: 20162738.

13. Herrmann E, Call J, Hernández-lloreda MV, Hare B, Herrmann E, Call J, et al. Humans have evolved specialized skills of social cognition: the cultural intelligence hypothesis. Science. 2007;317: 1360–1366. doi: 10.1126/science.1146282 17823346

14. Tomasello M. Great apes and human development: a personal history. Child Dev Perspect. 2018;12: 189–193. doi: 10.1111/cdep.12281

15. Martins EP, Hansen TF. The statistical analysis of interspecific data: a review and evaluation of phylogenetic comparative methods. In: Martins EP, editor. Phylogenies and the comparative method in animal behaviour. Oxford: Oxford University Press; 1995.

16. Fitch WT, Huber L, Bugnyar T. Social cognition and the evolution of language: constructing cognitive phylogenies. Neuron. 2010;65: 795–814. doi: 10.1016/j.neuron.2010.03.011 20346756

17. Fernandes HBF, Woodley MA, te Nijenhuis J. Differences in cognitive abilities among primates are concentrated on G: phenotypic and phylogenetic comparisons with two meta-analytical databases. Intelligence. 2014;46: 311–322. doi: 10.1016/j.intell.2014.07.007

18. Freckleton RP, Harvey PH, Pagel M. Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat. 2002;160: 712–726. doi: 10.1086/343873 18707460

19. Deaner RO, van Schaik CP, Johnson V. Do some taxa have better domain-general cognition than others? A meta-analysis of nonhuman primate studies. Evol Psychol. 2006;4: 149–196. doi: 10.1177/147470490600400114

20. Simons DJ. The value of direct replication. Perspect Psychol Sci. 2014;9: 76–80. doi: 10.1177/1745691613514755 26173243

21. Frank MC, Bergelson E, Bergmann C, Cristia A, Floccia C, Gervain J, Hamlin JK, Hannon EE, Kline M, Levelt C, Lew‐Williams C. A collaborative approach to infant research: Promoting reproducibility, best practices, and theory‐building. Infancy. 2017; 22: 421–35.

22. Klein RA, Ratliff KA, Vianello M, Adams RB, Bahník Š, Bernstein MJ, et al. Investigating variation in replicability: a “many labs” replication project. Soc Psychol. 2014;45: 142–152. doi: 10.1027/1864-9335/a000178

23. Moshontz H, Campbell L, Ebersole CR, IJzerman H, Urry HL, Forscher PS, et al. The Psychological Science Accelerator: advancing psychology through a distributed collaborative network. Adv Methods Pract Psychol Sci. 2018;1: 501–515. doi: 10.1177/2515245918797607

24. Amici F, Aureli F, Call J. Fission-fusion dynamics, behavioral flexibility, and inhibitory control in primates. Curr Biol. 2008;18: 1415–1419. doi: 10.1016/j.cub.2008.08.020 18804375

25. Amici F, Visalberghi E, Call J. Lack of prosociality in great apes, capuchin monkeys and spider monkeys: convergent evidence from two different food distribution tasks. Proc R Soc B Biol Sci. 2014;281: 20141699. doi: 10.1098/rspb.2014.1699 25209941

26. Amici F, Call J, Watzek J, Brosnan S, Aureli F. Social inhibition and behavioural flexibility when the context changes: a comparison across six primate species. Sci Rep. 2018;8: 3067. doi: 10.1038/s41598-018-21496-6 29449670

27. Burkart JM, Allon O, Amici F, Fichtel C, Finkenwirth C, Heschl A, et al. The evolutionary origin of human hyper-cooperation. Nat Commun. 2014;5: 4747. doi: 10.1038/ncomms5747 25158760

28. Alloway TP, Gathercole SE, Willis C, Adams AM. A structural analysis of working memory and related cognitive skills in young children. J Exp Child Psychol. 2004;87: 85–106. doi: 10.1016/j.jecp.2003.10.002 14757066

29. Engle RW, Tuholski SW, Laughlin JE, Conway ARA. Working memory, short-term memory, and general fluid intelligence: a latent-variable approach. J Exp Psychol Gen. 1999;128: 309–331. doi: 10.1037/0096-3445.128.3.309 10513398

30. Gathercole SE, Pickering SJ, Ambridge B, Wearing H. The structure of working memory from 4 to 15 years of age. Dev Psychol. 2004;40: 177–190. doi: 10.1037/0012-1649.40.2.177 14979759

31. D’Esposito M, Postle BR, Ballard D, Lease J. Maintenance versus manipulation of information held in working memory: an event-related fMRI study. Brain Cogn. 1999;41: 66–86. doi: 10.1006/brcg.1999.1096 10536086

32. Eldreth DA, Patterson MD, Porcelli AJ, Biswal BB, Rebbechi D, Rypma B. Evidence for multiple manipulation processes in prefrontal cortex. Brain Res. 2006;1123: 145–156. doi: 10.1016/j.brainres.2006.07.129 17070786

33. Owen AM, Downes JJ, Sahakian BJ, Polkey CE, Robbins TW. Planning and spatial working memory following frontal lobe lesions in man. Neuropsychologia. 1990;28: 1021–1034. doi: 10.1016/0028-3932(90)90137-d 2267054

34. Smith EE, Jonides J. Storage and executive processes in the frontal lobes. Science. 1999;283: 1657–1661. doi: 10.1126/science.283.5408.1657 10073923

35. Goldman-Rakic PS. Cellular basis of working memory. Neuron. 1995;14: 477–485. doi: 10.1016/0896-6273(95)90304-6 7695894

36. Tinklepaugh OL. The multiple delayed reaction with chimpanzees and monkeys. J Comp Psychol. 1932;13: 207–243. doi: 10.1037/h0072368

37. Nissen HW, Riesen AH, Nowlis V. Delayed response and discrimination learning by chimpanzees. J Comp Psychol. 1938;26: 361–386.

38. Barth J, Call J. Tracking the displacement of objects: a series of tasks with great apes (Pan troglodytes, Pan paniscus, Gorilla gorilla, and Pongo pygmaeus) and young children (Homo sapiens). J Exp Psychol Anim Behav Process. 2006;32: 239–252. doi: 10.1037/0097-7403.32.3.239 16834492

39. Harlow HF, Uehling H, Maslow AH. Comparative behavior of primates. Comp Psychol. 1932;13: 241–252.

40. Elmore LC, Wright AA. Monkey visual short-term memory directly compared to humans. J Exp Psychol Anim Learn Cogn. 2015;41: 32–38. doi: 10.1037/xan0000050 25706544

41. Elmore LC, Ji Ma W, Magnotti JF, Leising KJ, Passaro AD, Katz JS, et al. Visual short-term memory compared in rhesus monkeys and humans. Curr Biol. 2011;21: 975–979. doi: 10.1016/j.cub.2011.04.031 21596568

42. Buschman TJ, Siegel M, Roy JE, Miller EK. Neural substrates of cognitive capacity limitations. Proc Natl Acad Sci. 2011;108: 11252–11255. doi: 10.1073/pnas.1104666108 21690375

43. Hedden T, Gabrieli JDE. Insights into the ageing mind: a view from cognitive neuroscience. Nat Rev Neurosci. 2004;5: 87–96. doi: 10.1038/nrn1323 14735112

44. Bartus RT, Fleming D, Johnson HR. Aging in the rhesus monkey: debilitating effects on short-term memory. Journals Gerontol. 1978;33: 858–871. doi: 10.1093/geronj/33.6.858 106081

45. R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2018.

46. Bates DM, Maechler M, Bolker BM, Walker SC, Mächler M, Bolker BM, et al. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67: 1–48. doi: 10.18637/jss.v067.i01

47. Lenth R V. Emmeans: estimated marginal means, aka least-squares means. In: R package version 1.2.4. 2018.

48. Revell LJ. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol. 2012;3: 217–223. doi: 10.1111/j.2041-210X.2011.00169.x

49. Maclean EL, Matthews LJ, Hare BA, Nunn CL. How does cognition evolve? Phylogenetic comparative psychology. Anim Cogn. 2012;15: 223–238. doi: 10.1007/s10071-011-0448-8 21927850

50. Arnold C, Matthews LJ, Nunn CL. The 10kTrees website: a new online resource for primate phylogeny. Evol Anthropol. 2010;19: 114–118. doi: 10.1002/evan.20251

51. Yerkes RM, Yerkes DN. Concerning memory in the chimpanzee. J Comp Psychol. 1928;8: 237–271. doi: 10.1037/h0073804

52. Maier NRF. Delayed reaction and memory in rats. Pedagog Semin J Genet Psychol. 1929;36: 538–550. doi: 10.1080/08856559.1929.10532212

53. Hunter WS. The delayed reaction in animals and children. Behav Monograhs. 1913;2: 1–85.

54. Bohn M. ManyPrimates—Promoting large-scale collaboration across labs in primate cognition. 27th International Primatological Society Congress. Nairobi, Kenya; 2018.

55. Hopper LM. ManyPrimates: a new multinational, multi-institutional, multi-species collaborative effort to study primate cognition and behavior. 15th Midwest Primate Interest Group Annual Meeting. USA, Bloomington; 2018.

56. Brooks DR, Mayden RL, McLennan DA. Phylogeny and biodiversity: conserving our evolutionary legacy. Trends Ecol Evol. 1992;7: 55–59. doi: 10.1016/0169-5347(92)90107-M 21235951

57. Li B, Li M, Li J, Fan P, Ni Q, Lu J, et al. The primate extinction crisis in China: immediate challenges and a way forward. Biodivers Conserv. 2018;27: 3301–3327. doi: 10.1007/s10531-018-1614-y

58. Yamanashi Y, Hayashi M. Assessing the effects of cognitive experiments on the welfare of captive chimpanzees (Pan troglodytes) by direct comparison of activity budget between wild and captive chimpanzees. Am J Primatol. 2011;73: 1231–1238. doi: 10.1002/ajp.20995 21905060

59. Whitehouse J, Micheletta J, Powell LE, Bordier C, Waller BM. The impact of cognitive testing on the welfare of group housed primates. PLoS One. 2013;8: e78308. doi: 10.1371/journal.pone.0078308 24223146

60. Ross SR. How cognitive studies help shape our obligation for ethical care of chimpanzees. In: Lonsdorf E V., Ross SR, Atsuzawa T, editors. The mind of the chimpanzees: ecological and experimental perspectives. Chicago: The University of Chicago Press; 2010. pp. 309–319.

61. Clark FE. Cognitive enrichment and welfare: current approaches and future directions. Anim Behav Cogn. 2017;4: 52–71. doi: 10.12966/abc.05.02.2017

62. Washburn DA, Rumbaugh DM. Investigations of rhesus monkey video-task performance: evidence for enrichment. J Am Assoc Lab Anim Sci. 1992;31: 6–10.

63. Yamanashi Y, Matsuzawa T. Emotional consequences when chimpanzees (Pan troglodytes) face challenges: individual differences in self-directed behaviours during cognitive tasks. Anim Welf. 2010;19: 25–30.

64. Cronin KA, Jacobson SL, Bonnie KE, Hopper LM. Studying primate cognition in a social setting to improve validity and welfare: a literature review highlighting successful approaches. PeerJ. 2017;5: 3649. doi: 10.7717/peerj.3649 28791199

65. Ruby S, Buchanan-Smith HM. The effects of individual cubicle research on the social interactions and individual behavior of brown capuchin monkeys (Sapajus apella). Am J Primatol. 2015;77: 1097–1108. doi: 10.1002/ajp.22444 26173706

66. Hopper LM, Shender MA, Ross SR. Behavioral research as physical enrichment for captive chimpanzees. Zoo Biol. 2016;35: 293–297. doi: 10.1002/zoo.21297 27232752

67. Jacobson S. L, Kwiatt AC, Ross SR, Cronin KA. The effects of cognitive testing on the welfare of zoo-housed Japanese macaques (Macaca fuscata). Appl Anim Behav Sci. in prep.

Článek vyšel v časopise


2019 Číslo 10
Nejčtenější tento týden