Animal Cognition

, Volume 17, Issue 3, pp 503–515 | Cite as

Lemurs and macaques show similar numerical sensitivity

  • Sarah M. JonesEmail author
  • John Pearson
  • Nicholas K. DeWind
  • David Paulsen
  • Ana-Maria Tenekedjieva
  • Elizabeth M. BrannonEmail author
Original Paper


We investigated the precision of the approximate number system (ANS) in three lemur species (Lemur catta, Eulemur mongoz, and Eulemur macaco flavifrons), one Old World monkey species (Macaca mulatta) and humans (Homo sapiens). In Experiment 1, four individuals of each nonhuman primate species were trained to select the numerically larger of two visual arrays on a touchscreen. We estimated numerical acuity by modeling Weber fractions (w) and found quantitatively equivalent performance among all four nonhuman primate species. In Experiment 2, we tested adult humans in a similar procedure, and they outperformed the four nonhuman species but showed qualitatively similar performance. These results indicate that the ANS is conserved over the primate order.


Nonhuman primates Numerical cognition Comparative psychology Number discrimination Weber fraction Prosimians 



We thank the Duke Lemur Center, Monica Carlson, and the many research assistants who assisted with this research. We thank members of the Brannon laboratory for their helpful discussion of these data. This work was supported by a National Science Foundation CAREER award (No. 0448250) to Elizabeth M. Brannon.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

The experiments reported here comply with the current laws of the United States of America.

Supplementary material

10071_2013_682_MOESM1_ESM.pdf (215 kb)
Supplementary material 1 (PDF 214 kb)


  1. Agrillo C, Miletto Petrazzini ME (2012) The importance of replication in comparative psychology: the lesson of elephant quantity judgments. Front Psychol 3:181PubMedCentralPubMedGoogle Scholar
  2. Agrillo C, Dadda M, Serena G, Bisazza A (2008) Do fish count? Spontaneous discrimination of quantity in female mosquitofish. Anim Cogn doi. doi: 10.1007/s10071-008-0140-9 Google Scholar
  3. Agrillo C, Miletto Petrazzini ME, Tagliapietra C, Bisazza A (2012a) Inter-specific differences in numerical abilities among teleost fish. Front Psychol 3:483. doi: 10.3389/fpsyg.2012.00483 PubMedCentralPubMedGoogle Scholar
  4. Agrillo C, Piffer L, Bisazza A, Butterworth B (2012b) Evidence for two numerical systems that are similar in humans and guppies. PLoS ONE 7(2):e31923PubMedCentralPubMedCrossRefGoogle Scholar
  5. Anderson JR, Mitchell RW (1999) Macaques but not lemurs co-orient visually with humans. Folia Primatol 70:17–22PubMedCrossRefGoogle Scholar
  6. Beran MJ (2008) The evolutionary and developmental foundations of mathematics. PLoS Biol 6:e19PubMedCentralPubMedCrossRefGoogle Scholar
  7. Beran MJ, Johnson-Pynn JS, Ready C (2008) Quantity representation in children and rhesus monkeys: linear versus logarithmic scales. J Exp Child Psychol 100:225–233PubMedCentralPubMedCrossRefGoogle Scholar
  8. Beran MJ, Decker S, Schwartz A, Schultz N (2011a) Monkeys (Macaca mulatta and Cebus apella) and human adults and children (Homo sapiens) compare subsets of moving stimuli based on numerosity. Front Psychol 2:61. doi: 10.3389/fpsyg.2011.00061 PubMedCentralPubMedCrossRefGoogle Scholar
  9. Beran MJ, Johnson-Pynn JS, Ready C (2011b) Comparing children’s (Homo sapiens) and chimpanzees’ (Pan troglodytes) quantity judgments of sequentially presented sets of items. Curr Zool 57:419–428Google Scholar
  10. Best NG, Cowles MK, Vines K (1995) CODA* convergence diagnosis and output analysis software for Gibbs sampling output Version 0.30. MRC Biostatistics Unit, CambridgeGoogle Scholar
  11. Blakeslee B, Jacobs GH (1985) Color vision in the ring-tailed lemur (Lemur catta). Brain Behav Evol 26:154–166PubMedCrossRefGoogle Scholar
  12. Bond AB, Kamil AC, Balda RP (2003) Social complexity and transitive inference in corvids. Anim Behav 65:479–487CrossRefGoogle Scholar
  13. Brannon EM (2006) The representation of numerical magnitude. Curr Opin Neurobiol 16:222–229PubMedCentralPubMedCrossRefGoogle Scholar
  14. Brannon EM, Terrace HS (1998) Ordering of the numerosities 1 to 9 by monkeys. Science 282(5389):746–749PubMedCrossRefGoogle Scholar
  15. Brannon EM, Terrace HS (2000) Representation of the numerosities 1–9 by rhesus macaques (Macaca mulatta). J Exp Psychol Anim Behav Process 26(1):31–49PubMedCrossRefGoogle Scholar
  16. Cantlon JF, Brannon EM (2006) Shared system for ordering small and large numbers in monkeys and humans. Psychol Sci 17(5):401–406PubMedCrossRefGoogle Scholar
  17. Cantlon JF, Brannon EM (2007) Basic math in monkeys and college students. PLoS Biol 5(12):e328PubMedCentralPubMedCrossRefGoogle Scholar
  18. Cowles MK, Carlin BP (1996) Markov chain Monte Carlo convergence diagnostics: a comparative review. J Am Stat Assoc 91(434):883–904CrossRefGoogle Scholar
  19. Curtis DJ, Zaramody A (1998) Group size, home range use, and seasonal variation in the ecology of Eulemur mongoz. Int J Primatol 19(5):811–835CrossRefGoogle Scholar
  20. Deppe AM, Wright PC, Szelistowski WA (2009) Object permanence in lemurs. Anim Cogn 12(2):381–388PubMedCrossRefGoogle Scholar
  21. DeWind NK, Brannon EM (2012) Malleability of the approximate number system: effects of feedback and training. Front Hum Neurosci 6:68. doi: 10.3389/fnhum.2012.00068 PubMedCentralPubMedCrossRefGoogle Scholar
  22. Erhart EM, Overdorff DJ (2008) Spatial memory during foraging in prosimian primates: Propithecus edwardsi and Eulemur fulvus rufus. Folia Primatol 79:185–196PubMedCrossRefGoogle Scholar
  23. Feigenson L (2005) A double dissociation in infants’ representation of object arrays. Cognition 95:B37–B48PubMedCrossRefGoogle Scholar
  24. Feigenson L, Carey S (2003) Tracking individuals via object-files: evidence from infants’ manual search. Dev Sci 6:568–584CrossRefGoogle Scholar
  25. Feigenson L, Carey S, Hauser M (2002) The representations underlying infants’ choice of more: object-files versus analog magnitudes. Psychol Sci 13:150–156PubMedCrossRefGoogle Scholar
  26. Fichtel C, Kappeler PM (2010) Human universals and primate symplesiomorphies: Establishing the lemur baseline. In: Kappeler PM, Silk J (eds) Mind the gap: tracing the origins of human universals. Springer, HeidelbergGoogle Scholar
  27. Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, OxfordGoogle Scholar
  28. Gebuis T, Reynvoet B (2012) The role of visual information in numerosity estimation. PLoS ONE 7(5):e37426. doi: 10.1371/journal.pone.0037426 PubMedCentralPubMedCrossRefGoogle Scholar
  29. Gelman A, Hill J (2007) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, CambridgeGoogle Scholar
  30. Gelman A, Carlin JB, Stern HS, Rubin DB (2004) Bayesian data analysis. Chapman & Hall/CRC, Boca Raton, FLGoogle Scholar
  31. Genty E, Palmier C, Roeder J (2004) Learning to suppress responses to the larger of two rewards in two species of lemurs, Eulemur fulvus and E. macaco. Anim Behav 67(5):925–932CrossRefGoogle Scholar
  32. Gilmore C, Attridge N, Inglis M (2011) Measuring the approximate number system. Q J Exp Psychol 64(11):2099–2109CrossRefGoogle Scholar
  33. Gosset D, Roeder J (2000) Colour and shape discrimination in black lemurs (Eulemur macaco). Folia Primatol 71:173–176PubMedCrossRefGoogle Scholar
  34. Halberda J, Feigenson L (2008) Developmental change in the acuity of the “Number Sense”: the approximate number system in 3-, 4-, 5-, 6-year-olds and adults. Dev Psychol 44(5):1457–1465PubMedCrossRefGoogle Scholar
  35. Hanus D, Call J (2007) Discrete quantity judgments in the great apes (Pan paniscus, Pan troglodytes, Gorilla gorilla, Pongo pygmaeus): the effect of presenting whole sets versus item-by-item. J Comp Psychol 121(3):241–249PubMedCrossRefGoogle Scholar
  36. Hauser MD, Carey S, Hauser LB (2000) Spontaneous number representation in semi-free-ranging rhesus monkeys. Proc R Soc 267:829–833CrossRefGoogle Scholar
  37. Horvath JE, Weisrock DW, Embry SL, Fiorentino I, Balhoff JP, Kappeler P, Wray GA, Willard HF, Yoder AD (2008) Development and application of a phylogenomic toolkit: resolving the evolutionary history of Madagascar’s lemurs. Genome Res 18:489–499PubMedCentralPubMedCrossRefGoogle Scholar
  38. Houle D (1991) Genetic covariance of fitness correlates: what genetic correlations are made of and why it matters. Evolution 45:630–648CrossRefGoogle Scholar
  39. Houle D (1992) Comparing the evolvability and variability of quantitative traits. Genetics 130:195–204PubMedCentralPubMedGoogle Scholar
  40. Irie N, Hasegawa T (2012) Summation by Asian elephants (Elephas maximus). Behav Sci 2:50–56. doi: 10.3390/bs2020050 CrossRefGoogle Scholar
  41. Irie-Sugimoto N, Kobayashi T, Sato T, Hasegawa T (2009) Relative quantity judgment by Asian elephants (Elephas maximus). Anim Cogn 12:193–199. doi: 10.1007/s10071-008-0185-9 PubMedCrossRefGoogle Scholar
  42. Jacobs GH, Deegan JF (1993) Photopigments underlying color vision in ringtail lemurs (Lemur catta) and brown lemurs (Eulemur fulvus). Am J Primatol 30(3):243–256CrossRefGoogle Scholar
  43. Jacobs GH, Deegan JF (2003) Diurnality and cone photopigment polymorphism in strepsirrhines: examination of linkage in Lemur catta. Am J Phys Anthropol 122(1):66–72PubMedCrossRefGoogle Scholar
  44. Jones SM, Brannon EM (2012) Prosimian primates show ratio dependence in spontaneous quantity discriminations. Front Psychol 3:550. doi: 10.3389/fpsyg.2012.00550 PubMedCentralPubMedGoogle Scholar
  45. Jordan K, Brannon EM (2006a) A common representational system governed by Weber’s law: nonverbal numerical similarity judgments in six-year-old children and rhesus macaques. J Exp Child Psychol 95:215–229PubMedCrossRefGoogle Scholar
  46. Jordan K, Brannon EM (2006b) Weber’s Law influences numerical representations in rhesus macaques (Macaca mulatta). Anim Cogn 9(3):159–172PubMedCrossRefGoogle Scholar
  47. Kass R, Raftery A (1995) Bayes factors. J Am Stat Assoc 90:773–795CrossRefGoogle Scholar
  48. Leonhardt SD, Tung J, Camden JB, Leal M, Drea CM (2008) Seeing red: behavioral evidence of trichromatic color vision in strepsirrhine primates. Behav Ecol 20(1):1–12CrossRefGoogle Scholar
  49. Lewis KP, Jaffe S, Brannon EM (2005) Analog number representations in mongoose lemurs (Eulemur mongoz): evidence from a search task. Anim Cogn 8(4):247–252PubMedCrossRefGoogle Scholar
  50. Luhrs ML, Dammhahn M, Kappeler PM, Fichtel C (2009) Spatial memory in the grey mouse lemur (Microcebus murinus). Anim Cogn 12:599–609PubMedCentralPubMedCrossRefGoogle Scholar
  51. MacLean E, Merritt D, Brannon EM (2008) Social complexity predicts transitive reasoning in prosimian primates. Anim Behav 76:479–486PubMedCentralPubMedCrossRefGoogle Scholar
  52. MacLean E, Sandel A, Bray J, Oldenkamp R, Reddy R, Hare B (2013) Group size predicts social but not nonsocial cognition in lemurs. PLos One 8(6):e66359. doi: 10.1371/journal.pone.0066359
  53. Merritt D, MacLean EL, Jaffe S, Brannon EM (2007) A comparative analysis of serial ordering in ring-tailed lemurs (Lemur catta). J Comp Psychol 121(4):363–371PubMedCentralPubMedCrossRefGoogle Scholar
  54. Merritt D, MacLean E, Crawford JC, Brannon EM (2011) Numerical rule-learning in ring-tailed lemurs (Lemur catta). Front Comp Psychol 2(23):1–9Google Scholar
  55. Mousseau TA, Roff DA (1987) Natural selection and the heritability of fitness components. Heredity 59:181–197PubMedCrossRefGoogle Scholar
  56. Perdue BM, Talbot CF, Stone A, Beran MJ (2012) Putting the elephant back in the herd: Elephant relative quantity judgments match those of other species. Anim Cogn 15(5):955–961. doi: 10.1007/s10071-012-0521-y Google Scholar
  57. Piazza M, Izard V (2009) How humans count: numerosity and the parietal cortex. Neuroscientist 15(3):261–273PubMedCrossRefGoogle Scholar
  58. Piazza M, Izard V, Pinel P, Le Bihan D, Dehaene S (2004) Tuning curves for approximate numerosity in the human intraparietal sulcus. Neuron 44:547–555PubMedCrossRefGoogle Scholar
  59. Pica P, Lemer C, Izard V, Dehaene S (2004) Exact and approximate arithmetic in an Amazonian indigene group. Science 306(5695):499–503PubMedCrossRefGoogle Scholar
  60. Picq JL (1993) Radial maze performance in young and aged grey mouse lemurs (Microcebus murinus). Primates 24:223–226CrossRefGoogle Scholar
  61. Picq JL (2007) Aging affects executive functions and memory in mouse lemur primates. Exp Gerontol 42:223–232PubMedCrossRefGoogle Scholar
  62. Platt ML, Brannon EM, Briese TL, French JA (1996) Differences in feeding ecology predict differences in performance between golden lion tamarins (Leontopithecus rosalia) and Wied’s marmosets (Callithrix Kuhli) on spatial and visual memory tasks. Anim Learn Behav 24:384–393CrossRefGoogle Scholar
  63. Roff DA, Mousseau TA (1987) Quantitative genetics and fitness: lessons from Drosophila. Heredity 58:103–118PubMedCrossRefGoogle Scholar
  64. Rosati AG, Stevens JR, Hare B, Hauser MD (2007) The evolutionary origins of human patience: temporal preferences in chimpanzees, bonobos, and human adults. Curr Biol 17:1663–1668PubMedCrossRefGoogle Scholar
  65. Ruiz A, Gomez JC, Roeder JJ, Byrne RW (2009) Gaze following and gaze priming in lemurs. Anim Cogn 12:427–434PubMedCrossRefGoogle Scholar
  66. Rumbaugh DM, Arnold RC (1971) Learning: a comparative study of lemur and cercopithecus. Folia Primatol 14:154–160PubMedCrossRefGoogle Scholar
  67. Sandel AA, MacLean E, Hare B (2011) Evidence from four lemur species that ringtailed lemur social cognition converges with that of haplorhine primates. Anim Behav 81:925–931CrossRefGoogle Scholar
  68. Santos LR, Barnes JL, Mahajan N (2005a) Expectations about numerical events in four lemur species (Eulemur fulvus, Eulemur mongoz, Lemur catta and Varecia rubra). Anim Cogn 8(4):253–262PubMedCrossRefGoogle Scholar
  69. Santos LR, Mahajan N, Barnes JL (2005b) How prosimian primates represent tools: experiments with two lemur species (Eulemur fulvus and Lemur catta). J Comp Psychol 119(4):394–403PubMedCrossRefGoogle Scholar
  70. Sauther ML, Sussman RW, Gould L (1999) The socioecology of the ringtailed lemur: thirty-five years of research. Evol Anthro 8(4):120–132CrossRefGoogle Scholar
  71. Savage A, Snowdon CT (1989) Apples and oranges: the pitfalls of comparative intelligence. Behav Brain Sci 12(3):605–606CrossRefGoogle Scholar
  72. Scarf D, Hayne H, Colombo M (2011) Pigeons on par with primates in numerical competence. Science 334(6063):1664PubMedCrossRefGoogle Scholar
  73. Shepherd SV, Platt ML (2008) Spontaneous social orienting and gaze following in ringtailed lemurs (Lemur catta). Anim Cogn 11:13–20PubMedCrossRefGoogle Scholar
  74. Tattersall I (1982) The primates of Madagascar. Columbia University Press, New YorkGoogle Scholar
  75. Tomasello M, Hare B, Fogleman T (2001) The ontogeny of gaze following in chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta). Anim Behav 61:335–343CrossRefGoogle Scholar
  76. Uller C, Lewis J (2009) Horses (Equus caballus) select the greater of two quantities in small numerical contrasts. Anim Cogn 12(5):733–738PubMedCrossRefGoogle Scholar
  77. Uller C, Jaeger R, Guidry G, Martin C (2003) Salamanders (Plethodon cinereus) go for more: rudiments of number in an amphibian. Anim Cogn 6:105–112PubMedCrossRefGoogle Scholar
  78. Veilleux CC, Kirk EC (2009) Visual acuity in the cathemeral strepsirrhine Eulemur macaco flavifrons. Am J Primatol 71(4):343–352PubMedCrossRefGoogle Scholar
  79. Volampeno MSN, Masters JC, Downs CT (2011) Home range size in the blue-eyed black lemur (Eulemur flavifrons): a comparison between dry and wet seasons. Mamm Biol 76(2):157–164CrossRefGoogle Scholar
  80. Wagenmakers EJ, Lodewyckx T, Kuriyal H, Grasman R (2010) Bayesian hypothesis testing for psychologists: a tutorial on the Savage–Dickey method. Cogn Psychol 60:158–189PubMedCrossRefGoogle Scholar
  81. Wood JN, Hauser MD, Glynn DD, Barner D (2008) Free-ranging rhesus monkeys spontaneously individuate and enumerate small numbers of non-solid portions. Cognition 106:207–221PubMedCrossRefGoogle Scholar
  82. Wynn K (1992) Addition and subtraction by human infants. Nature 358:749–750PubMedCrossRefGoogle Scholar
  83. Yoder AD (2007) Lemurs: a quick guide. Curr Biol 17(20):866–868CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Sarah M. Jones
    • 1
    • 5
    Email author
  • John Pearson
    • 2
    • 3
    • 4
  • Nicholas K. DeWind
    • 2
    • 3
  • David Paulsen
    • 1
  • Ana-Maria Tenekedjieva
    • 2
  • Elizabeth M. Brannon
    • 1
    • 2
    Email author
  1. 1.Department of Psychology and NeuroscienceDuke UniversityDurhamUSA
  2. 2.Center for Cognitive NeuroscienceDuke UniversityDurhamUSA
  3. 3.Department of NeurobiologyDuke University Medical CenterDurhamUSA
  4. 4.Division of NeurosurgeryDuke University Medical CenterDurhamUSA
  5. 5.Psychology DepartmentSt. Norbert CollegeDe PereUSA

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