Animal Cognition

, Volume 21, Issue 6, pp 813–820 | Cite as

Quantity discrimination in fish species: fish use non-numerical continuous quantity traits to select shoals

  • Wei Xiong
  • Lian-Chun Yi
  • Zhonghua Tang
  • Xin Zhao
  • Shi-Jian FuEmail author
Original Paper


Fish typically prefer to live in big shoals due to the associated ecological benefits. Shoaling is a behavior that depends on the ability to quantitatively discriminate. The fundamental mechanism involved in quantity discrimination determines whether fish can discriminate a shoal using numerical discrete cues (e.g., number of shoal members), non-numerical continuous traits (e.g., total body surface area) or both; however, the mechanism is currently a controversial topic. In the present study, we used a spontaneous choice experiment to test whether guppy (Poecilia reticulata), zebrafish (Danio rerio), Chinese crucian carp (Carassius auratus) and qingbo (Spinibarbus sinensis) rely on continuous (i.e., body surface area) or discrete (i.e., number of shoal members) information for shoal selection by altering the body surface area (cumulative body surface area ratio of 3:2 or 1:1) between two stimulus shoals with a different number of members (2 individuals vs 3 individuals). All four fish species preferred to shoal with the stimulus shoal with the larger cumulative surface area even if the shoal had fewer members; however, fish showed no shoal preference when the cumulative surface body areas of both stimulus shoals were equal. Furthermore, qingbo did not numerically discriminate between a shoal with 1 individual and a shoal with 3 individuals when the cumulative surface areas of both stimulus shoals were equal; however, qingbo showed a preference for the shoal with the larger cumulative surface area when the two stimulus shoals each had 3 individuals. In conclusion, the present study demonstrated that all four fish species relied only on non-numerical continuous quantity information for shoal selection, at least under a difficult task (i.e., 2 vs 3).


Continuous variables Fish species Numerical cue Quantity discrimination Spontaneous choice experiment 



This work was supported by the National Natural Science Foundation of China (no. 31670418).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

10071_2018_1214_MOESM1_ESM.xlsx (35 kb)
Supplementary material 1 (XLSX 35 KB)


  1. Agrillo C, Bisazza A (2014) Spontaneous vs. trained numerical abilities. A comparison between the two main tools to study numerical competence in non-human animals. J Neurosci Methods 234:82–91CrossRefGoogle Scholar
  2. Agrillo C, Dadda M, Bisazza A (2007) Quantity discrimination in female mosquitofish. Anim Cogn 10:63–70CrossRefGoogle Scholar
  3. Agrillo C, Dadda M, Serena G, Bisazza A (2008) Do fish count? Spontaneous discrimination of quantity in female mosquitofish. Anim Cogn 11:495–503CrossRefGoogle Scholar
  4. Agrillo C, Dadda M, Serena G, Bisazza A (2009) Use of number by fish. PLoS One 4:e4786CrossRefGoogle Scholar
  5. Agrillo C, Piffer L, Bisazza A (2011) Number versus continuous quantity in numerosity judgments by fish. Cognition 119:281–287CrossRefGoogle Scholar
  6. Agrillo C, Miletto Petrazzini ME, Tagliapietra C, Bisazza A (2012a) Inter-specific differences in numerical abilities among teleost fish. Front Psychol 3:483PubMedPubMedCentralGoogle Scholar
  7. 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):e31923CrossRefGoogle Scholar
  8. Beran MJ (2008) The evolutionary and developmental foundations of mathematics. PLoS Biol 6:e19CrossRefGoogle Scholar
  9. Bisazza A, Tagliapietra C, Bertolucci C, Foà A, Agrillo C (2014) Non-visual numerical discrimination in a blind cavefish (Phreatichthys andruzzii). J Exp Biol 217:1902–1909CrossRefGoogle Scholar
  10. Croft DP, Arrowsmith BJ, Bielby J, Skinner K, White E, Couzin ID, Magurran AE, Ramnarine I, Krause J (2003) Mechanisms underlying shoal composition in the Trinidadian guppy, Poecilia reticulate. Oikos 100:429–438CrossRefGoogle Scholar
  11. Davis H, Pérusse R (1988) Numerical competence in animals: definitional issues, current evidence, and a new research agenda. Behav Brain Sci 11:561–579CrossRefGoogle Scholar
  12. DeLong CM, Barbato S, O’Leary T, Wilcox KT (2017) Small and large number discrimination in goldfish (Carassius auratus) with extensive training. Behav Proc 141:172–183CrossRefGoogle Scholar
  13. Dhillon RS, Yao L, Matey V, Chen BJ, Zhang AJ, Cao ZD, Fu SJ, Brauner CJ, Wang YS, Richards JG (2013) Interspecific differences in hypoxia-induced gill remodeling in carp. Physiol Biochem Zool 86:727–739CrossRefGoogle Scholar
  14. Emmerton J, Renner JC (2006) Scalar effects in the visual discrimination of numerosity by pigeons. Learn Behav 34:176–192CrossRefGoogle Scholar
  15. Feigenson L, Dehaene S, Spelke E (2004) Core systems of number. Trends Cogn Sci 8:307–314CrossRefGoogle Scholar
  16. Foster WA, Treherne JE (1981) Evidence for the dilution effect in the selfish herd from fish predation on a marine insect. Nature 293:466–467CrossRefGoogle Scholar
  17. Frommen JG, Hiermes M, Bakker TCM (2009) Disentangling the effects of group size and density on shoaling decisions of threespined sticklebacks (Gasterosteus aculeatus). Behav Ecol Sociobiol 63:1141–1148CrossRefGoogle Scholar
  18. Gebuis T, Reynvoet B (2012) The interplay between nonsymbolic number and its continual visual properties. J Exp Psychol General 141:642–648CrossRefGoogle Scholar
  19. Gómez-Laplaza LM, Gerlai R (2013a) The role of body surface area in quantity discrimination in angelfish (Pterophyllum scalare). PLoS One 8(12):e83880CrossRefGoogle Scholar
  20. Gómez-Laplaza LM, Gerlai R (2013b) Quantification abilities in angelfish (Pterophyllum scalare): the influence of continuous variables. Anim Cogn 16:373–383CrossRefGoogle Scholar
  21. Hager MC, Helfman GS (1991) Safety in numbers: shoal size choice by minnows under predatory threat. Behav Ecol Sociobiol 29:271–276CrossRefGoogle Scholar
  22. Hauser MD, Carey S, Hauser LB (2000) Spontaneous number representation in semi-free-ranging rhesus monkeys. Proc R Soc London Ser B 267:829–833CrossRefGoogle Scholar
  23. Karoubi N, Leibovich T, Segev R (2017) Symbol-value association and discrimination in the archerfish. PLoS One 12(4):e0174044CrossRefGoogle Scholar
  24. Kilian A, Yaman S, Fersen L, Güntürkün O (2003) A bottle nose dolphin (Tursiops truncates) discriminates visual stimuli differing in numerosity. Learn Behav 31:133–142CrossRefGoogle Scholar
  25. Killen SS, Fu C, Wu QY, Wang YX, Fu SJ (2016) The relationship between metabolic rate and sociability is altered by food deprivation. Funct Ecol 30:1358–1365CrossRefGoogle Scholar
  26. Krusche P, Uller C, Dicke U (2010) Quantity discrimination in salamanders. J Exp Biol 213:1822–1828CrossRefGoogle Scholar
  27. Landeau L, Terborgh J (1986) Oddity and the confusion effect in predation. Anim Behav 34:1372–1380CrossRefGoogle Scholar
  28. Ledesma JM, McRobert SP (2008) Shoaling in juvenile guppies: the effects of body size and shoal size. Behav Process 77:384–388CrossRefGoogle Scholar
  29. Lucon-Xiccato T, Dadda M (2017) Individual guppies differ in quantity discrimination performance across antipredator and foraging contexts. Behav Ecol Sociobiol 71:13CrossRefGoogle Scholar
  30. Lucon-Xiccato T, Miletto Petrazzini ME, Agrillo C, Bisazza A (2015) Guppies discriminate between two quantities of food items but prioritize item size over total amount. Anim Behav 107:183–191CrossRefGoogle Scholar
  31. Lucon-Xiccato T, Dadda M, Gatto E, Bisazza A (2017) Development and testing of a rapid method for measuring shoal size discrimination. Anim Cogn 20:149–157CrossRefGoogle Scholar
  32. Matsuzawa T (2009) Symbolic representation of number in chimpanzees. Curr Opin Neurobiol 19:92–98CrossRefGoogle Scholar
  33. McComb K, Packer C, Pusey A (1994) Roaring and numerical assessment in contests between groups of female lions, Panthera leo. Anim Behav 47:379–387CrossRefGoogle Scholar
  34. Mehlis M, Thünken T, Bakker TCM, Frommen JG (2015) Quantification acuity in spontaneous shoaling decisions of three-spined sticklebacks. Anim Cogn 18:1125–1131CrossRefGoogle Scholar
  35. Miletto Petrazzini ME, Agrillo C (2016) Turning to the larger shoal: are there individual differences in small- and large-quantity discrimination of guppies? Ethol Ecol Evol 28:211–220Google Scholar
  36. Miller N, Gerlai R (2012) From schooling to shoaling: patterns of collective motion in zebrafish (Danio rerio). PLoS One 7(11):e48865CrossRefGoogle Scholar
  37. Pérez-Escudero A, Vicente-Page J, Hinz RC, Arganda S, De Polavieja GG (2014) idTracker: tracking individuals in a group by automatic identification of unmarked animals. Nat Methods 11:743–748CrossRefGoogle Scholar
  38. Peuhkuri N (1999) Size-assorted fish shoals and the majority’s choice. Behav Ecol Sociobiol 46:307–312CrossRefGoogle Scholar
  39. Pisa PE, Agrillo C (2009) Quantity discrimination in felines: a preliminary investigation of the domestic cat (Felis silvestris catus). J Ethol 27:289–293CrossRefGoogle Scholar
  40. Pulliam HR (1973) On the advantages of flocking. J Theor Biol 38:419–422CrossRefGoogle Scholar
  41. Quattrini FG, Bshary R, Roche DG (2018) Does the presence of an odd individual affect group choice? Behav Ecol 29:855–861CrossRefGoogle Scholar
  42. Rugani R, Fontanari L, Simoni E, Regolin L, Vallortigara G (2009) Arithmetic in newborn chicks. Proc R Soc London Ser B 276:2451–2460CrossRefGoogle Scholar
  43. Sokal RR, Rohlf FJ (1995) Biometry. Freeman and Company, New YorkGoogle Scholar
  44. Stevens JR, Wood JN, Hauser MD (2007) When quantity trumps number: discrimination experiments in cotton-top tamarins (Saguinus oedipus) and common marmosets (Callithrix jacchus). Anim Cogn 10:429–437CrossRefGoogle Scholar
  45. Tang ZH, Fu SJ (2016) Numerical discrimination of juvenile qingbo improved by shoaling. J Chongqing Norm Univ (Natural Science Edition) 33:32–36Google Scholar
  46. Tang ZH, Wu H, Huang Q, Kuang L, Fu SJ (2017) The shoaling behavior of two cyprinid species in conspecific and heterospecific groups. Peer J 5:e3397CrossRefGoogle Scholar
  47. West RE, Young RJ (2002) Do domestic dogs show any evidence of being able to count? Anim Cogn 5:183–186CrossRefGoogle Scholar
  48. Wong BBM, Rosenthal GG (2005) Shoal choice in swordtails when preferences conflict. Ethology 111:179–186CrossRefGoogle Scholar
  49. Xu F, Spelke ES (2000) Large number discrimination in 6-month-old infants. Cognition 74:B1–B11CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratory of Evolutionary Physiology and Behavior, Chongqing Key Laboratory of Animal BiologyChongqing Normal UniversityChongqingChina

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