The Evolution of Primate Short-Term Memory

Animal Behavior and Cognition, vol. 9, pp. 428–516

Abstract

Short-term memory is implicated in a range of cognitive abilities and is critical for understanding primate cognitive evolution. To investigate the effects of phylogeny, ecology and sociality on short-term memory, we tested the largest and most diverse primate sample to date (421 non-human primates across 41 species) in an experimental delayed-response task. Our results confirm previous findings that longer delays decrease memory performance across species and taxa. Our analyses demonstrate a considerable contribution of phylogeny over ecological and social factors on the distribution of short-term memory performance in primates; closely related species had more similar short-term memory abilities. Overall, individuals in the branch of Hominoidea performed better compared to Cercopithecoidea, who in turn performed above Platyrrhini and Strepsirrhini. Interdependencies between phylogeny and socioecology of a given species presented an obstacle to disentangling the effects of each of these factors on the evolution of short-term memory capacity. However, this study offers an important step forward in understanding the interspecies and individual variation in short-term memory ability by providing the first phylogenetic reconstruction of this trait’s evolutionary history. The dataset constitutes a unique resource for studying the evolution of primate cognition and the role of short-term memory in other cognitive abilities.

Authors 81

1. ManyPrimates

   Max Planck Institute for Human Development

   Affiliation as printed

   Center for Adaptive Rationality , Max Planck Institute for Human Development ;

   Center for Adaptive Rationality, Max Planck Institute for Human Development;

2. Géraud Aguenounon

   Laboratoire de Neurosciences Cognitives et Adaptatives · Université de Strasbourg

   Affiliation as printed

   Centre de Primatologie de l ' Université de Strasbourg ;

   Laboratoire de Neurosciences Cognitives et Adaptatives , Université de Strasbourg ;

   Centre de Primatologie de l'Université de Strasbourg;

   Laboratoire de Neurosciences Cognitives et Adaptatives, Université de Strasbourg;

3. Matthias Allritz

   University of St Andrews

   Affiliation as printed

   School of Psychology and Neuroscience , University of St Andrews ;

   School of Psychology and Neuroscience, University of St Andrews;

4. Drew Altschul

   University of Edinburgh

   Affiliation as printed

   Department of Psychology , The University of Edinburgh ;

   Department of Psychology, The University of Edinburgh;

5. Sébastien Ballesta

   Laboratoire de Neurosciences Cognitives et Adaptatives · Université de Strasbourg

   Affiliation as printed

   Centre de Primatologie de l ' Université de Strasbourg ;

   Laboratoire de Neurosciences Cognitives et Adaptatives , Université de Strasbourg ;

   Centre de Primatologie de l'Université de Strasbourg;

   Laboratoire de Neurosciences Cognitives et Adaptatives, Université de Strasbourg;

6. Alice Beaud

   Laboratoire de Neurosciences Cognitives et Adaptatives · Université de Strasbourg

   Affiliation as printed

   Centre de Primatologie de l ' Université de Strasbourg ;

   Laboratoire de Neurosciences Cognitives et Adaptatives , Université de Strasbourg ;

   Centre de Primatologie de l'Université de Strasbourg;

   Laboratoire de Neurosciences Cognitives et Adaptatives, Université de Strasbourg;

7. Manuel Bohn

   Max Planck Society · Max Planck Institute for Evolutionary Anthropology

   Affiliation as printed

   Max Planck Institute for Evolutionary Anthropology ;

   Max Planck Institute for Evolutionary Anthropology;

8. Sally L. Bornbusch

   Duke University

   Affiliation as printed

   Department of Evolutionary Anthropology , Duke University ;

   Department of Evolutionary Anthropology, Duke University;

9. Angela Brandão

   University of Lisbon

   Affiliation as printed

   Animal Behavior Department , University of Lisbon ;

   Center for Philosophy of Sciences , University of Lisbon ;

   Animal Behavior Department, University of Lisbon;

   Center for Philosophy of Sciences, University of Lisbon;

10. Thomas Bugnyar

    University of Vienna

    Affiliation as printed

    Department of Behavioral and Cognitive Biology , University of Vienna ;

    Department of Behavioral and Cognitive Biology, University of Vienna;

11. Judith Maria Burkart

    University of Zurich

    Affiliation as printed

    Department of Anthropology , University of Zurich ; 12 Inkawu Vervet Project , South Africa;

    Department of Anthropology, University of Zurich;

12. Léa Bustamante

    Laboratoire de Neurosciences Cognitives et Adaptatives · Université de Strasbourg

    Affiliation as printed

    Centre de Primatologie de l ' Université de Strasbourg ;

    Laboratoire de Neurosciences Cognitives et Adaptatives , Université de Strasbourg ;

    Centre de Primatologie de l'Université de Strasbourg;

    Laboratoire de Neurosciences Cognitives et Adaptatives, Université de Strasbourg;

13. Josep Call

    University of Edinburgh

    Affiliation as printed

    Department of Psychology , The University of Edinburgh ;

    Department of Psychology, The University of Edinburgh;

14. Charlotte Canteloup

    University of Lausanne

    Affiliation as printed

    University of Lausanne ; 14 Wuhan Zoo , Wuhan , China;

    Inkawu Vervet Project, South Africa;

    University of Lausanne; 14 Wuhan Zoo, Wuhan, China;

15. Chuangshi Cao

    Max Planck Institute for Human Development

    Affiliation as printed

    Center for Adaptive Rationality , Max Planck Institute for Human Development ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

16. Kai R. Caspar

    University of Duisburg-Essen

    Affiliation as printed

    Department of General Zoology , University of Duisburg-Essen ;

    Department of General Zoology, University of Duisburg-Essen;

17. Diana da Silva

    University of Lisbon

    Affiliation as printed

    Primate Cognition Research Group , Center for Philosophy of Sciences , University of Lisbon ;

    Primate Cognition Research Group, Center for Philosophy of Sciences, University of Lisbon;

18. Alexandra Allison de Sousa

    Bath Spa University

    Affiliation as printed

    Bath Spa University ;

    Bath Spa University;

19. Sarah E. DeTroy

    Max Planck Society · Max Planck Institute for Evolutionary Anthropology

    Affiliation as printed

    Max Planck Institute for Evolutionary Anthropology ;

    Max Planck Institute for Evolutionary Anthropology;

20. Shona Duguid

    University of St Andrews

    Affiliation as printed

    School of Psychology and Neuroscience , University of St Andrews ;

    School of Psychology and Neuroscience, University of St Andrews;

21. Timothy M. Eppley

    Portland State University · Zoological Society of San Diego

    Affiliation as printed

    Conservation Science & Wildlife Health , San Diego Zoo Wildlife Alliance ;

    Department of Anthropology , Portland State University ;

    Conservation Science & Wildlife Health, San Diego Zoo Wildlife Alliance;

    Department of Anthropology, Portland State University;

22. Claudia Fichtel

    German Primate Center

    Affiliation as printed

    Behavioral Ecology & Sociobiology Unit , German Primate Center -Leibniz Institute for Primate Research ;

    Behavioral Ecology & Sociobiology Unit, German Primate Center -Leibniz Institute for Primate Research;

23. Julia Fischer

    German Primate Center

    Affiliation as printed

    Cognitive Ethology Laboratory , German Primate Center -Leibniz Institute for Primate Research ;

    Cognitive Ethology Laboratory, German Primate Center -Leibniz Institute for Primate Research;

24. James A. Grange

    Keele University

    Affiliation as printed

    School of Psychology , Keele University ;

    School of Psychology, Keele University;

25. Nicholas M. Grebe

    Duke University

    Affiliation as printed

    Department of Evolutionary Anthropology , Duke University ;

    Department of Evolutionary Anthropology, Duke University;

26. Daniel Hanus

    Max Planck Society · Max Planck Institute for Evolutionary Anthropology

    Affiliation as printed

    Max Planck Institute for Evolutionary Anthropology ;

    Max Planck Institute for Evolutionary Anthropology;

27. Daniel B. M. Haun

    Max Planck Society · Max Planck Institute for Evolutionary Anthropology

    Affiliation as printed

    Max Planck Institute for Evolutionary Anthropology ;

    Max Planck Institute for Evolutionary Anthropology;

28. Lou Haux

    German Primate Center

    Affiliation as printed

    Cognitive Ethology Laboratory , German Primate Center -Leibniz Institute for Primate Research ;

    Cognitive Ethology Laboratory, German Primate Center -Leibniz Institute for Primate Research;

29. Yseult Héjja‐Brichard

    Max Planck Institute for Human Development

    Affiliation as printed

    Center for Adaptive Rationality , Max Planck Institute for Human Development ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

30. Annabella Helman

    Centre National de la Recherche Scientifique · École Pratique des Hautes Études · Duke University · Université de Montpellier · Centre d'Écologie Fonctionnelle et Évolutive · Institut de Recherche pour le Développement

    Affiliation as printed

    Department of Evolutionary Anthropology , Duke University ;

    Centre d'Ecologie Fonctionnelle et Evolutive, Université de Montpellier, CNRS, EPHE, IRD, Montpellier;

    Department of Evolutionary Anthropology, Duke University;

31. István Hernádi

    University of Pecs

    Affiliation as printed

    UP-Gedeon Richter Grastyan Translational Research Center , University of Pecs ;

    UP-Gedeon Richter Grastyan Translational Research Center, University of Pecs;

32. Raquel Adriana Hernandez-Aguilar

    University of Oslo · Universitat de Barcelona

    Affiliation as printed

    Centre for Ecological and Evolutionary Synthesis , Department of Biosciences , University of Oslo ;

    Department of Social Psychology and Quantitative Psychology , Serra Hunter Programme , University of Barcelona ;

    Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo;

    Department of Social Psychology and Quantitative Psychology, Serra Hunter Programme, University of Barcelona;

33. Esther Herrmann

    University of Portsmouth

    Affiliation as printed

    Centre for Comparative and Evolutionary Psychology , Department of Psychology , University of Portsmouth ;

    Centre for Comparative and Evolutionary Psychology, Department of Psychology, University of Portsmouth;

34. Lydia M. Hopper

    Johns Hopkins University · Johns Hopkins Medicine · Lincoln Park Zoo

    Affiliation as printed

    Department of Molecular and Comparative Pathobiology , Johns Hopkins University School of Medicine ;

    Lester E. Fisher Center for the Study and Conservation of Apes , Lincoln Park Zoo ;

    Department of Molecular and Comparative Pathobiology, Johns Hopkins University School of Medicine;

    Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo;

35. Lauren E. Howard

    Franklin & Marshall College

    Affiliation as printed

    Department of Psychology , Scientific and Philosophical Studies of the Mind , Franklin & Marshall College ;

    Department of Psychology, Scientific and Philosophical Studies of the Mind, Franklin & Marshall College;

36. Lei Huang

    Max Planck Institute for Human Development

    Affiliation as printed

    Center for Adaptive Rationality , Max Planck Institute for Human Development ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

37. Sarah M. Huskisson

    Lincoln Park Zoo

    Affiliation as printed

    Lester E. Fisher Center for the Study and Conservation of Apes , Lincoln Park Zoo ;

    Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo;

38. Ivo F. Jacobs

    Lund University

    Affiliation as printed

    Department of Philosophy / Cognitive Science , Lund University ;

    Lund University Primate Research Station ;

    Department of Philosophy / Cognitive Science, Lund University;

    Lund University Primate Research Station;

39. Zhiyong Jin

    Duke Kunshan University · East China Normal University

    Affiliation as printed

    Phylo-Cognition Laboratory , Division of Natural and Applied Sciences , Duke Kunshan University , Duke Institute for Brain Sciences ;

    Shanghai Key Laboratory of Brain Functional Genomics , School of Psychology and Cognitive Science , East China Normal University ;

    Phylo-Cognition Laboratory, Division of Natural and Applied Sciences, Duke Kunshan University, Duke Institute for Brain Sciences;

    Shanghai Key Laboratory of Brain Functional Genomics, School of Psychology and Cognitive Science, East China Normal University;

40. Marine Joly

    Universitat de Barcelona

    Affiliation as printed

    Department of Social Psychology and Quantitative Psychology , Serra Hunter Programme , University of Barcelona ;

    Department of Social Psychology and Quantitative Psychology, Serra Hunter Programme, University of Barcelona;

41. Fumihiro Kano

    University of Konstanz

    Affiliation as printed

    University of Konstanz ; 37 Kumamoto Sanctuary , Kumamoto , Japan;

    University of Konstanz; 37 Kumamoto Sanctuary, Kumamoto, Japan;

42. Stefanie Keupp

    German Primate Center

    Affiliation as printed

    Cognitive Ethology Laboratory , German Primate Center -Leibniz Institute for Primate Research ;

    Cognitive Ethology Laboratory, German Primate Center -Leibniz Institute for Primate Research;

43. Evelin Kiefer

    University of Pecs

    Affiliation as printed

    UP-Gedeon Richter Grastyan Translational Research Center , University of Pecs ;

    UP-Gedeon Richter Grastyan Translational Research Center, University of Pecs;

44. Balázs Knakker

    University of Pecs

    Affiliation as printed

    UP-Gedeon Richter Grastyan Translational Research Center , University of Pecs ;

    UP-Gedeon Richter Grastyan Translational Research Center, University of Pecs;

45. Katalin Kóczán

    University of Pecs

    Affiliation as printed

    UP-Gedeon Richter Grastyan Translational Research Center , University of Pecs ;

    UP-Gedeon Richter Grastyan Translational Research Center, University of Pecs;

46. Larissa Kraus

    Max Planck Society · Max Planck Institute for Evolutionary Anthropology

    Affiliation as printed

    Max Planck Institute for Evolutionary Anthropology ;

    Max Planck Institute for Evolutionary Anthropology;

47. Sze Chai Kwok

    Duke Kunshan University · Shanghai Changning Mental Health Center · East China Normal University

    Affiliation as printed

    Phylo-Cognition Laboratory, Division of Natural and Applied Sciences, Duke Kunshan University, Duke Institute for Brain Sciences;

    Shanghai Changning Mental Health Center, Shanghai, China;

    Shanghai Key Laboratory of Brain Functional Genomics, School of Psychology and Cognitive Science, East China Normal University;

    Shanghai Key Laboratory of Magnetic Resonance, East China Normal University;

48. Marie Lefrançois

    Laboratoire de Neurosciences Cognitives et Adaptatives · Université de Strasbourg

    Affiliation as printed

    Centre de Primatologie de l ' Université de Strasbourg ;

    Laboratoire de Neurosciences Cognitives et Adaptatives , Université de Strasbourg ;

    Centre de Primatologie de l'Université de Strasbourg;

    Laboratoire de Neurosciences Cognitives et Adaptatives, Université de Strasbourg;

49. Siyi Liu

    Peking University

    Affiliation as printed

    School of Psychological and Cognitive Sciences , Beijing Key Laboratory of Behavior and Mental Health , Peking University ;

    School of Psychological and Cognitive Sciences, Beijing Key Laboratory of Behavior and Mental Health, Peking University;

50. Miquel Llorente

    Universitat de Girona

    Affiliation as printed

    Serra Húnter Fellow, Department of Psychology , University of Girona ;

    Serra Húnter Fellow, Department of Psychology, University of Girona;

51. Elizabeth V. Lonsdorf

    Emory University · Franklin & Marshall College

    Affiliation as printed

    Department of Anthropology , Emory University ;

    Department of Psychology ,

    Biological Foundations of Behavior Program, Franklin & Marshall College;

    Department of Anthropology, Emory University;

    Department of Psychology,

52. Louise Loyant

    University of Portsmouth

    Affiliation as printed

    Centre for Comparative and Evolutionary Psychology , Department of Psychology , University of Portsmouth ;

    Centre for Comparative and Evolutionary Psychology, Department of Psychology, University of Portsmouth;

53. Katarzyna Majecka

    University of Łódź

    Affiliation as printed

    The Natural History Museum , Faculty of Biology and Environmental Protection , University of Lodz ;

    The Natural History Museum, Faculty of Biology and Environmental Protection, University of Lodz;

54. Luke Maurits

    Max Planck Society · Max Planck Institute for Evolutionary Anthropology · Max Planck Institute for Human Development

    Affiliation as printed

    Max Planck Institute for Evolutionary Anthropology ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

55. Hélène Meunier

    Laboratoire de Neurosciences Cognitives et Adaptatives · Max Planck Institute for Human Development · Université de Strasbourg

    Affiliation as printed

    Centre de Primatologie de l ' Université de Strasbourg ;

    Laboratoire de Neurosciences Cognitives et Adaptatives , Université de Strasbourg ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

56. Flávia Mobili

    University of Zurich

    Affiliation as printed

    Department of Anthropology , University of Zurich ;

    Department of Anthropology, University of Zurich;

57. Luca Morino

    Muséum national d'Histoire naturelle

    Affiliation as printed

    Muséum National d'Histoire Naturelle , Paris , France;

    Muséum National d'Histoire Naturelle, Paris, France;

58. Alba Motes‐Rodrigo

    Max Planck Institute for Human Development

    Affiliation as printed

    Center for Adaptive Rationality , Max Planck Institute for Human Development ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

59. Vincent Nijman Aachen

    Leiden University · Oxford Brookes University · University of Veterinary Medicine Vienna · Ghent University · University of Łódź · University of Neuchâtel · University of Lausanne

    Affiliation as printed

    School of Social Science , Oxford Brookes University ; 50 Department of Ecology and ManyPrimates et al. 429 Vertebrate Zoology, Faculty of Biology and Environmental Protection, University of Lodz; 51 Normandie University; 52 Department of Zoology, Faculty of Science, University of South Bohemia; 53 Institute of Psychology, Leiden University; 54 Institute of Biology, University of Neuchâtel; 55 Department of Experimental Psychology, Ghent University; 56 Comparative Cognition, Messerli Research Institute, University of Veterinary Medicine Vienna; 57 University of St. Andrews; 58 California National Primate Research Center

    Department of Ecology and Evolution, University of Lausanne;

    School of Social Science, Oxford Brookes University; 50 Department of Ecology and Vertebrate Zoology, Faculty of Biology and Environmental Protection, University of Lodz; 51 Normandie University; 52 Department of Zoology, Faculty of Science, University of South Bohemia; 53 Institute of Psychology, Leiden University; 54 Institute of Biology, University of Neuchâtel; 55 Department of Experimental Psychology, Ghent University; 56 Comparative Cognition, Messerli Research Institute, University of Veterinary Medicine Vienna; 57 University of St. Andrews; 58 California National Primate Research Center

60. Caroline Ihomi

    Laboratoire de Neurosciences Cognitives et Adaptatives · Max Planck Institute for Human Development · Université de Strasbourg

    Affiliation as printed

    Centre de Primatologie de l ' Université de Strasbourg ;

    Laboratoire de Neurosciences Cognitives et Adaptatives , Université de Strasbourg ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

61. Tomas Persson

    Lund University

    Affiliation as printed

    Department of Philosophy / Cognitive Science , Lund University ;

    Lund University Primate Research Station ;

    Department of Philosophy / Cognitive Science, Lund University;

    Lund University Primate Research Station;

62. Dariusz Pietraszewski

    Max Planck Institute for Human Development

    Affiliation as printed

    Center for Adaptive Rationality , Max Planck Institute for Human Development ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

63. Juan Felipe Reátiga Parrish

    Max Planck Institute for Human Development

    Affiliation as printed

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

64. Anthony Roig

    Max Planck Institute for Human Development · Université de Strasbourg

    Affiliation as printed

    Centre de Primatologie de l ' Université de Strasbourg ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

65. Alejandro Sánchez-Amaro

    Max Planck Society · Max Planck Institute for Evolutionary Anthropology · Max Planck Institute for Human Development

    Affiliation as printed

    Max Planck Institute for Evolutionary Anthropology ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

66. Yutaro Sato

    Max Planck Institute for Human Development · Wildlife Research Center, Kyoto University

    Affiliation as printed

    Wildlife Research Center , Kyoto University ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

67. Gabriela-Alina Sauciuc

    Lund University · Max Planck Institute for Human Development

    Affiliation as printed

    Department of Philosophy / Cognitive Science , Lund University ;

    Lund University Primate Research Station ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

68. Allie E. Schrock

    Duke University · Max Planck Institute for Human Development

    Affiliation as printed

    Department of Evolutionary Anthropology , Duke University ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

69. Manon K. Schweinfurth

    University of St Andrews · Max Planck Institute for Human Development

    Affiliation as printed

    School of Psychology and Neuroscience , University of St Andrews ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

70. Amanda M. Seed

    University of St Andrews · Max Planck Institute for Human Development

    Affiliation as printed

    School of Psychology and Neuroscience , University of St Andrews ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

71. Caroline L. Shearer

    Duke University · Max Planck Institute for Human Development

    Affiliation as printed

    Department of Evolutionary Anthropology , Duke University ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

72. Vedrana Šlipogor

    University of Vienna

    Affiliation as printed

    Department of Behavioral and Cognitive Biology , University of Vienna ;

    Department of Behavioral and Cognitive Biology, University of Vienna;

73. Yanjie Su

    Peking University · Max Planck Institute for Human Development

    Affiliation as printed

    School of Psychological and Cognitive Sciences , Beijing Key Laboratory of Behavior and Mental Health , Peking University ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

74. Kirsten Sutherland

    Max Planck Society · Max Planck Institute for Evolutionary Anthropology · Max Planck Institute for Human Development

    Affiliation as printed

    Max Planck Institute for Evolutionary Anthropology ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

75. Jingzhi Tan

    Max Planck Institute for Human Development

    Affiliation as printed

    Center for Adaptive Rationality , Max Planck Institute for Human Development ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

76. Derry Taylor

    Max Planck Institute for Human Development

    Affiliation as printed

    Center for Adaptive Rationality , Max Planck Institute for Human Development ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

77. Camille Aurélie Troisi

    Max Planck Institute for Human Development

    Affiliation as printed

    Center for Adaptive Rationality , Max Planck Institute for Human Development ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

78. Christoph Johannes Völter

    University of St Andrews · Franklin & Marshall College · Max Planck Institute for Human Development

    Affiliation as printed

    Biological Foundations of Behavior Program , Franklin & Marshall College ;

    School of Psychology and Neuroscience , University of St Andrews ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

79. Elizabeth Warren

    Max Planck Institute for Human Development

    Affiliation as printed

    Center for Adaptive Rationality , Max Planck Institute for Human Development ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

80. Julia Watzek

    Max Planck Institute for Human Development

    Affiliation as printed

    Center for Adaptive Rationality , Max Planck Institute for Human Development ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;

81. Pauline Zablocki‐Thomas

    Max Planck Institute for Human Development

    Affiliation as printed

    Center for Adaptive Rationality , Max Planck Institute for Human Development ;

    Center for Adaptive Rationality, Max Planck Institute for Human Development;