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Animal Cognition

, Volume 22, Issue 2, pp 133–143 | Cite as

Numerical ability in fish species: preference between shoals of different sizes varies among singletons, conspecific dyads and heterospecific dyads

  • Yang Bai
  • Zhong-Hua Tang
  • Shi-Jian FuEmail author
Original Paper

Abstract

Group living confers ecological benefits, and the associated fitness gain may be positively related to the size of the group. Thus, the ability to discriminate numerical differences may confer important fitness advantages in social fish. There is evidence that this ability can be improved by behavioral interactions among individuals of the same species. Here, we looked for this effect in both conspecific and heterospecific dyads. In Chinese bream and grass carp, we measured the sociability and shoal preferences of singletons, conspecific dyads and heterospecific dyads presented with different numerical comparisons (0 vs 8, 2 vs 8, 4 vs 8, 6 vs 8 and 8 vs 8). Chinese bream generally showed higher sociability than did grass carp, but grass carp in heterospecific dyads showed improved sociability that was similar to that of Chinese bream. Among the comparisons, both grass carp and Chinese bream singletons could only discriminate the comparison of 2 vs 8, suggesting lower quantitative abilities in these fish species compared to other fish species. Grass carp dyads were more successful in discriminating between 6 and 8 than were singletons, although no such improvement was observed in their discrimination between 4 and 8. In contrast, numerical ability did not vary between singletons and conspecific dyads in Chinese bream. More interestingly, Chinese bream and grass carp in heterospecific groups could discriminate between 4 and 8, but neither species showed a preference when presented with 6 and 8. Our results suggested that interaction between conspecific grass carp might improve their joint numerical ability, and a similar process might occur in Chinese bream in heterospecific dyads. However, the mechanism underlying the differences in improvements in numerical ability requires further investigation. The improved cognitive ability of heterospecific dyads might yield important fitness advantages for predator avoidance and efficient foraging in the wild.

Keywords

Numerical ability Cyprinid Collective intelligence Shoal preference Meritocratic leadership Many-wrongs principle 

Notes

Acknowledgements

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

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References

  1. Abaid N, Porfiri M (2012) Leader–follower consensus over numerosity-constrained random networks. Automatica 48:1845–1851CrossRefGoogle Scholar
  2. Agrillo C, Dadda M (2007) Discrimination of the larger shoal in the poeciliid fish Girardinus falcatus. Ethol Ecol Evol 19:145–157CrossRefGoogle 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, Piffer L, Bisazza A, Butterworth B (2012) Evidence for two numerical systems that are similar in humans and guppies. PLoS One 7(2):e31923CrossRefPubMedCentralGoogle Scholar
  5. Ashraf I, Bradshaw H, Ha T-T, Halloy J, Godoy-Diana R, Thiria B (2017) Simple phalanx pattern leads to energy saving in cohesive fish schooling. Proc Natl Acad Sci USA 114:9599–9604CrossRefGoogle Scholar
  6. Bisazza A, Butterworth B, Piffer L, Bahrami B, Miletto Petrazzini ME, Agrillo C (2014) Collective enhancement of numerical acuity by meritocratic leadership in fish. Sci Rep 4:4560CrossRefPubMedCentralGoogle Scholar
  7. Cattelan S, Lucon-Xiccato T, Pilastro A, Griggio M (2017) Is the mirror test a valid measure of fish sociability? Anim Behav 127:109–116CrossRefGoogle Scholar
  8. Cote J, Fogarty S, Sih A (2012) Individual sociability and choosiness between shoal types. Anim Behav 83:1469–1476CrossRefGoogle Scholar
  9. Dadda M, Piffer L, Agrillo C, Bisazza A (2009) Spontaneous number representation in mosquitofish. Cognition 112:343–348CrossRefGoogle Scholar
  10. Emmerton J, Renner JC (2006) Scalar effects in the visual discrimination of numerosity by pigeons. Learn Behav 34:176–192CrossRefGoogle Scholar
  11. Feigenson L, Dehaene S, Spelke E (2004) Core systems of number. Trends Cogn Sci 8:307–314CrossRefGoogle Scholar
  12. 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
  13. Frommen JG, Luz C, Bakker TC (2007) Nutritional state influences shoaling preference for familiars. Zoology (Jena) 110:369–376CrossRefGoogle Scholar
  14. Galton F (1907) Vox populi. Nature 75:450–451CrossRefGoogle Scholar
  15. Gebuis T, Reynvoet B (2012) The interplay between nonsymbolic number and its continual visual properties. J Exp Psychol Gen 141:642–648CrossRefGoogle Scholar
  16. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, OxfordGoogle Scholar
  17. Krause J, Ruxton GD, Krause S (2010) Swarm intelligence in animals and humams. Trends Ecol Evol 25:28–34CrossRefGoogle Scholar
  18. Krusche P, Uller C, Dicke U (2010) Quantity discrimination in salamanders. J Exp Biol 213:1822–1828CrossRefGoogle Scholar
  19. Landeau L, Terborgh J (1986) Oddity and the ‘confusion effect’ in predation. Anim Behav 34:1372–1380CrossRefGoogle Scholar
  20. Liu S, Fu SJ (2017) Effects of food availability on metabolism, behaviour, growth and their relationships in a triploid carp. J Exp Biol 220:4711CrossRefGoogle Scholar
  21. Lucon-Xiccato T, Bisazza A (2017) Individual differences in cognition among teleost fishes. Behav Proc 141:184–195CrossRefGoogle Scholar
  22. Lucon-Xiccato T, Dadda M (2017) Personality and cognition: sociability negatively predicts shoal size discrimination performance in guppies. Front Psychol 8:1118CrossRefPubMedCentralGoogle Scholar
  23. Lucon-Xiccato T, Dadda M, Gatto E, Bisazza A (2017) Development and testing of a rapid method for measuring shoal size discrimination. Anim Cogn 202:149–157CrossRefGoogle Scholar
  24. 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
  25. Miletto Petrazzini ME, Lucon-Xiccato T, Agrillo C, Bisazza A (2015) Use of ordinal information by fish. Sci Rep 5:15497CrossRefGoogle Scholar
  26. Miller NY, Gerlai R (2008) Oscillations in shoal cohesion in zebrafish (Danio rerio). Behav Brain Res 193:148–151CrossRefPubMedCentralGoogle Scholar
  27. Pérez-Escudero A, Vicente-Page J, Hinz RC, Arganda S, DePolavieja GG (2014) idTracker: tracking individuals in a group by automatic identification of unmarked animals. Nat Methods 11:743–748CrossRefGoogle Scholar
  28. 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
  29. Pitcher TJ, Magurran AE, Winfield IJ (1982) Fish in larger shoals find food faster. Behav Ecol Sociobiol 10:149–151CrossRefGoogle Scholar
  30. Polverino G, Abaid N, Kopman V, Macrì S, Porfiri M (2012) Zebrafish response to robotic fish: preference experiments on isolated individuals and small shoals. Bioinspiration Biomim 7(3):036019CrossRefGoogle Scholar
  31. Potrich D, Sovrano VA, Stancher GV, Vallortigara G (2015) Quantity discrimination by zebrafish (Danio rerio). Comp Psychol 129:388–393CrossRefGoogle Scholar
  32. Pritchard VL, Lawrence J, Butlin RK, Krause J (2001) Shoal choice in zebrafish, Danio rerio: the influence of shoal size and activity. Anim Behav 62:1085–1088CrossRefGoogle Scholar
  33. Pulliam HR (1973) On the advantages of flocking. J Theor Biol 38:419–422CrossRefGoogle Scholar
  34. Rieucau G, Giraldeau LA (2009) Group size effect caused by food competition in nutmeg mannikins (Lonchura punctulata). Behav Ecol 20:421–425CrossRefGoogle Scholar
  35. Rodgers GM, Kimbell H, Morrell LJ (2013) Mixed-phenotype grouping: the interaction between oddity and crypsis. Oecologia 172:59–68CrossRefGoogle Scholar
  36. Simons AM (2004) Many wrongs: the advantage of group navigation. Trends Ecol Evol 19:453–455CrossRefGoogle Scholar
  37. Tang ZH, Fu SJ (2016) Numerical discrimination of juvenile qingbo improved by shoaling. J Chongqing Norm Univ (Nat Sci Ed) 33:32–36Google Scholar
  38. 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
  39. Tang ZH, Wu QY, Fu SJ (2018) Inspection behaviour and inter-individual cooperation in juvenile qingbo: the effects of prior predator exposure and food deprivation. J Ethol 36:181–190CrossRefGoogle Scholar
  40. Thünken T, Eigster M, Frommen JG (2014) Context-dependent group size preferences in large shoals of three-spined sticklebacks. Anim Behav 90:205–210CrossRefGoogle Scholar
  41. Xu F, Spelke ES (2000) Large number discrimination in 6-month-old infants. Cognition 74:B1–B11CrossRefGoogle Scholar
  42. Zeng LQ, Fu C, Xi L, Peng JL, Fu SJ (2017) Phenotypic correlations and individual variation of energy metabolism and personality in juvenile Chinese bream (Parabramis pekinensis) Acta Ecol Sin 37:4807–4816Google 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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