Animal Cognition

, Volume 17, Issue 6, pp 1413–1419 | Cite as

Extensive training extends numerical abilities of guppies

  • Angelo Bisazza
  • Christian Agrillo
  • Tyrone Lucon-XiccatoEmail author
Short Communication


Recent studies on animal mathematical abilities suggest that all vertebrates show comparable abilities when they are given spontaneous preference tests, such as selecting the larger number of food items, but that mammals and birds generally achieve much better performance than fish when tested with training procedures. At least part of these differences might be due to the fact that fish are usually trained with only one or two dozen trials while extensive training, sometimes with thousands of trials, is normally performed in studies of mammals and birds. To test this hypothesis, female guppies were trained on four consecutive numerical discriminations of increasing difficulty (from 2 vs. 3 to 5 vs. 6 items), with up to 120 trials with each discrimination. Five out of eight subjects discriminated all contrasts up to 4 versus 5 objects at levels significantly better than chance, a much higher limit than the 2 versus 3 limit previously reported in studies that provided fish with only short training sequences. Our findings indicate that the difference in numerical cognition between teleosts and warm-blooded vertebrates might be smaller than previously supposed.


Numerical cognition Poecilia reticulata Training procedure Numerical acuity 



The authors would like to thank Michael J Beran for his useful comments and Michela Giovagnoni for her help in testing the animals. This work was funded by the FIRB grant (RBFR13KHFS) from Ministero dell’Istruzione, Università e Ricerca (MIUR, Italy) to Christian Agrillo. Experiments comply with all laws of the country (Italy) in which they were performed.

Supplementary material

Supplementary material 1 (AVI 15936 kb)


  1. Agrillo C, Bisazza A (2014) Spontaneous versus trained numerical abilities. A comparison between the two main tools to study numerical competence in non-human animals. J Neurosci Meth, online first. doi: 10.1016/j.jneumeth.2014.04.027
  2. Agrillo C, Dadda M, Serena G, Bisazza A (2008) Do fish count? Spontaneous discrimination of quantity in female mosquitofish. Anim Cogn 11:495–503PubMedCrossRefGoogle Scholar
  3. Agrillo C, Piffer L, Bisazza A (2010) Large number discrimination by fish. PLoS ONE 5(12):e15232PubMedCrossRefPubMedCentralGoogle Scholar
  4. Agrillo C, Piffer L, Bisazza A (2011) Number versus continuous quantity in numerosity judgments by fish. Cognition 119:281–287PubMedCrossRefGoogle Scholar
  5. Agrillo C, Miletto Petrazzini ME, Tagliapietra C, Bisazza A (2012a) Inter-specific differences in numerical abilities among teleost fish. Front Psych 3:483. doi: 10.3389/fpsyg.2012.00483 Google Scholar
  6. Agrillo C, Miletto Petrazzini ME, Piffer L, Dadda M, Bisazza A (2012b) A new training procedure for studying discrimination learning in fishes. Behav Brain Res 230:343–348PubMedCrossRefGoogle Scholar
  7. Agrillo C, Piffer L, Bisazza A, Butterworth B (2012c) Evidence for two numerical systems that are similar in humans and guppies. PLoS ONE 7(2):e31923PubMedCrossRefPubMedCentralGoogle Scholar
  8. Agrillo C, Miletto Petrazzini ME, Bisazza A (2014) Numerical acuity of fish is improved in the presence of moving targets, but only in the subitizing range. Anim Cogn 17(2):307–316PubMedCrossRefGoogle Scholar
  9. Al Aïn S, Giret N, Grand M, Kreutzer M, Bovet D (2009) The discrimination of discrete and continuous amounts in African grey parrots (Psittacus erithacus). Anim Cogn 12:145–154CrossRefGoogle Scholar
  10. Arsalidou M, Taylor MJ (2011) Is 2 + 2 = 4? Meta-analyses of brain areas needed for numbers and calculations. Neuroimage 54:2382–2393PubMedCrossRefGoogle Scholar
  11. Barnard AM, Hughes KD, Gerhardt RR, DiVincenti L Jr, Bovee JM, Cantlon JF (2013) Inherently analog quantity representations in olive baboons (Papio anubis). Front Psychol 4:253. doi: 10.3389/fpsyg.2013.00253 PubMedCrossRefPubMedCentralGoogle Scholar
  12. Beran MJ (2001) Summation and numerousness judgments of sequentially presented sets of items by chimpanzees (Pan troglodytes). J Comp Psychol 155:181–191CrossRefGoogle Scholar
  13. Beran MJ (2004) Chimpanzees (Pan troglodytes) respond to nonvisible sets after one-by-one addition and removal of items. J Comp Psychol 118:25–36PubMedCrossRefGoogle Scholar
  14. Beran MJ (2008a) Monkeys (Macaca mulatta and Cebus apella) track, enumerate, and compare multiple sets of moving items. J Exp Psych Anim Behav Proc 34:63–74CrossRefGoogle Scholar
  15. Beran MJ (2008b) The evolutionary and developmental foundations of mathematics. PLoS Biol 6:e19PubMedCrossRefPubMedCentralGoogle Scholar
  16. Bisazza A (2010) Cognition. In: Evans F, Pilastro A, Schlupp I (eds) Ecology and evolution of poeciliid fishes. Chicago University Press, Chicago, pp 165–173Google Scholar
  17. Bisazza A, Piffer L, Serena G, Agrillo C (2010) Ontogeny of numerical abilities in fish. PLoS ONE 5:e15516PubMedCrossRefPubMedCentralGoogle Scholar
  18. Brown C, Laland KN (2003) Social learning in fishes: a review. Fish Fish 4:280–288CrossRefGoogle Scholar
  19. Bshary R, Wickler W, Fricke H (2002) Fish cognition: a primate’s eye view. Anim Cogn 5:1–13PubMedCrossRefGoogle Scholar
  20. Cantlon JF, Brannon EM (2007) How much does number matter to a monkey (Macaca mulatta)? J Exp Psych Anim Behav Proc 33(1):32–41CrossRefGoogle Scholar
  21. Cantrell L, Smith LB (2013) Open questions and a proposal: a critical review of the evidence on infant numerical abilities. Cognition 128(3):331–352PubMedCrossRefPubMedCentralGoogle Scholar
  22. Cheek JM, Smith LR (1999) Music training and mathematics achievement. Adolescence 34:759–761PubMedGoogle Scholar
  23. Dadda M, Piffer L, Agrillo C, Bisazza A (2009) Spontaneous number representation in mosquitofish. Cognition 112:343–348PubMedCrossRefGoogle Scholar
  24. Emmerton J, Delius JD (1993) Beyond sensation: visual cognition in pigeons. In: Zeigler HP, Bischof H-J (eds) Vision, brain, and behavior in birds. MIT Press, Cambridge, MA, pp 377–390Google Scholar
  25. Feigenson L, Dehaene S, Spelke ES (2004) Core systems of number. Trends Cogn Sci 8:307–314PubMedCrossRefGoogle Scholar
  26. Gauthier I, Skudlarski P, Gore JC, Anderson AW (2000) Expertise for cars and birds recruits brain areas involved in face recognition. Nat Neurosci 3:191–197PubMedCrossRefGoogle Scholar
  27. Goldman M, Shapiro S (1979) Matching-to-sample and oddity-from sample in goldfish. J Exp Anal Behav 31:259–266PubMedCrossRefPubMedCentralGoogle Scholar
  28. Gómez-Laplaza LM, Gerlai R (2011) Spontaneous discrimination of small quantities: shoaling preferences in angelfish (Pterophyllum scalare). Anim Cogn 14:565–574PubMedCrossRefGoogle Scholar
  29. 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 Psych 44(5):1457–1465CrossRefGoogle Scholar
  30. 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 121:241–249PubMedCrossRefGoogle Scholar
  31. Hauser MD, Carey S, Hauser LB (2000) Spontaneous number representation in semi-free-ranging rhesus monkeys. Proc R Soc Lond B 267:829–833CrossRefGoogle Scholar
  32. Hunt S, Low J, Burns CK (2008) Adaptive numerical competency in a food-hoarding songbird. Proc R Soc Lond B 10:1098–1103Google Scholar
  33. Jaakkola K, Fellner W, Erb L, Rodriguez M, Guarino E (2005) Understanding of the concept of numerically ‘less’ by bottlenose dolphins (Tursiops truncatus). J Comp Psychol 119:286–303CrossRefGoogle Scholar
  34. Libertus ME, Feigenson L, Halberda J (2013) Is approximate number precision a stable predictor of math ability? Learn Indiv Differ 1(25):126–133CrossRefGoogle Scholar
  35. Pahl M, Si A, Zhang S (2013) Numerical cognition in bees and other insects. Front Psychol 4(162). doi: 10.3389/fpsyg.2013.00162
  36. Pepperberg IM (2006) Grey parrot numerical competence: a review. Anim Cogn 9:377–391PubMedCrossRefGoogle Scholar
  37. Piffer L, Agrillo C, Hyde DC (2012) Small and large number discrimination in guppies. Anim Cogn 15:215–221PubMedCrossRefGoogle Scholar
  38. Roberts WA, Mitchell S (1994) Can a pigeon simultaneously process temporal and numerical information? J Exp Psych Anim Behav Proc 20:66–78CrossRefGoogle Scholar
  39. Rodd F, Hughes K, Grether G, Baril C (2002) A possible non-sexual origin of mate preference: are male guppies mimicking fruit? Proc R Soc Lond B 269(1490):475–481CrossRefGoogle Scholar
  40. Schartl M, Walter RB, Shen Y, Garcia T, Catchen J, Amores A, Braasch I, Chalopin D, Volff JN, Lesch KP, Bisazza A, Minx P, Hillier L, Wilson RK, Fuerstenberg S, Boore J, Searle S, Postlethwait JH, Warren WC (2013) The genome of the platyfish, Xiphophorus maculatus, provides insights into evolutionary adaptation and several complex traits. Nat Genet 45:567–572PubMedCrossRefGoogle Scholar
  41. Sokal RR, Rohlf FJ (1995) Biometry: the principals and practice of statistics in biological research. WH Freeman and Company, New YorkGoogle Scholar
  42. Tomonaga M (2008) Relative numerosity discrimination by chimpanzees (Pan troglodytes): evidence for approximate numerical representations. Anim Cogn 11:43–57PubMedCrossRefGoogle Scholar
  43. Uller C, Jaeger R, Guidry G, Martin C (2003) Salamanders (Plethodon cinereus) go for more: rudiments of number in a species of basal vertebrate. Anim Cogn 6:105–112PubMedCrossRefGoogle Scholar
  44. Volff JN (2005) Genome evolution and biodiversity in teleost fish. Heredity 94:280–294PubMedCrossRefGoogle Scholar
  45. Wittbrodt J, Meyer A, Schartl M (1998) More genes in fish? BioEssays 20:511–515CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Angelo Bisazza
    • 1
  • Christian Agrillo
    • 1
  • Tyrone Lucon-Xiccato
    • 1
    Email author
  1. 1.Department of General PsychologyUniversity of PadovaPaduaItaly

Personalised recommendations