Behavioral Ecology and Sociobiology

, Volume 55, Issue 6, pp 561–568 | Cite as

Correlates of boldness in three-spined sticklebacks (Gasterosteus aculeatus)

  • Ashley J. W. WardEmail author
  • Philip Thomas
  • Paul J. B. Hart
  • Jens Krause
Original Article


Behavioural variation is known to occur between individuals of the same population competing for resources. Individuals also vary with respect to their boldness or shyness. An individual’s position along the shy-bold axis may be defined as the extent to which it is willing to trade off potentially increased predation risks for possible gains in resources. Similarly, group living may be interpreted as a trade-off between anti-predatory tactics and foraging efficiency. The responses of three-spined sticklebacks (Gasterosteus aculeatus) were tested across four social contexts to assess relative boldness or shyness and to further examine whether their behaviour would be consistent within and between contexts. Individuals displayed consistent responses within and between the first two contexts: those individuals which resumed foraging rapidly after a simulated aerial predator attack also displayed low shoaling tendencies. Such fish were deemed to be bold, whilst those which displayed the converse behaviour, slow resumption of foraging and a high shoaling tendency, were deemed to be shy. In a third context, bold individuals out-competed shy conspecifics for food. Boldness was also positively correlated with growth over a 6-week period. The position adopted by an individual within a group is usually interpreted as a trade-off between predation risk and foraging efficiency—both are greater at the front of a mobile group. Bold individuals showed significantly stronger tendencies towards front positions than shy conspecifics. The results suggest that, contrary to some previous studies on other animals, bold or shy behaviour in sticklebacks is consistent between contexts.


Gasterosteus aculeatus Bold Shy Shoaling Competition 



The authors would like to thank Tatiana Czeschlik, Neil Metcalfe and two anonymous referees for their time and comments which transformed this manuscript. In addition, the authors would like to thank Steve Ison for his valuable assistance over the course of this study. A.W. was funded by the National Environmental Research Council of the UK. These experiments comply with the current laws of the UK.


  1. Barber I, Ruxton GD (1998) Temporal prey distribution affects the competitive ability of parasitised sticklebacks. Anim Behav 58:1477–1483CrossRefGoogle Scholar
  2. Barnard CJ (1984) Producers and scroungers: strategies of exploitation and parasitism. Croom Helm, London, pp 95–125Google Scholar
  3. Budaev SV (1997) Alternative styles in the European wrasse, Symphodus ocellatus—boldness-related schooling tendency. Environ Biol Fish 49:71–78CrossRefGoogle Scholar
  4. Bumann D, Krause J (1993) Front individuals lead in shoals of 3-spined sticklebacks (Gasterosteus aculeatus) and juvenile roach (Rutilus rutilus). Behaviour 125:189–198Google Scholar
  5. Bumann D, Krause J, Rubenstein D (1997) Mortality risk of spatial positions in animal groups: the danger of being in the front. Behaviour 134:1034–1074Google Scholar
  6. Coleman K, Wilson DS (1998) Shyness and boldness in pumpkinseed sunfish—individual differences are context-specific. Anim Behav 56:927–936CrossRefPubMedGoogle Scholar
  7. Coleman K, Arendt J, Wilson DS (1998) Consistent differences in individual boldness; a frequency dependent behavior among pumpkinseed fish. Bull Ecol Soc Am 78:70Google Scholar
  8. 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 reticulata. Oikos 100:429–438Google Scholar
  9. DeBlois EM, Rose GA (1996) Cross-shoal variability in the feeding habits of migrating Atlantic cod (Gadus morhua). Oecologia 108:192–196Google Scholar
  10. Gill AB, Hart PJB (1996) Unequal competition between three-spined stickleback, Gasterosteus aculeatus, L, encountering sequential prey. Anim Behav 51:689–698CrossRefGoogle Scholar
  11. Godin J-GJ, Clark KAV (1997) Risk-taking in stickleback fishes faced with different predatory threats. Ecoscience 4:246–251Google Scholar
  12. Herskin J, Steffensen JF (1998) Energy savings in sea bass swimming in a school: measurements of tail beat frequency and oxygen consumption at different swimming speeds. J Fish Biol 53:366–376CrossRefGoogle Scholar
  13. Jezierski TA, Konecka AM (1996) Handling and rearing results in young rabbits. Appl Anim Behav Sci 46:243–250CrossRefGoogle Scholar
  14. Johnsson JI, Sernland E, Blixt M (2001) Sex-specific aggression and anti-predator behaviour in young brown trout. Ethology 107:587–599CrossRefGoogle Scholar
  15. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, OxfordGoogle Scholar
  16. Krause J, Reeves P, Hoare DJ (1998) Positioning behaviour in roach shoals—the role of body length and nutritional state. Behaviour 125:1031–1039Google Scholar
  17. Major P (1978) Predator-prey interactions in two schooling fishes, Caranx ignobilis and Stolephorus purpureus. Anim Behav 26:760–777Google Scholar
  18. Marchant-Forde JN (2002) Piglet- and stockperson-directed sow aggression after farrowing and the relationship with a pre-farrowing, human approach test. Appl Anim Behav Sci 75:115–132CrossRefGoogle Scholar
  19. McCune S (1995) The impact of paternity and early socialisation on the development of cats’ behaviour to people and novel objects. Appl Anim Behav Sci 45:109–124CrossRefGoogle Scholar
  20. Neill SRStJ, Cullen JM (1974) Experiments on whether schooling by their prey affects the hunting behaviour of cephalopod and fish predators. J Zool Lond 172:549–569Google Scholar
  21. Pitcher TJ (1986) Functions of shoaling behaviour in teleosts. In: Pitcher TJ (ed) The behaviour of teleost fishes. John Hopkins University Press, Baltimore, pp 294–337Google Scholar
  22. Reale D, Gallant BY, Leblanc M, Festa-Bianchet M (2000) Consistency of temperament in bighorn ewes and correlates with behaviour and life history. Anim Behav 60:589–597CrossRefPubMedGoogle Scholar
  23. Robinson B, Wilson DS (1994) Character release and displacement in fishes: a neglected literature. Am Nat 144:596–627CrossRefGoogle Scholar
  24. Rochette R, Tetreault F, Himmelman JH (2001) Aggregation of whelks, Buccinum undatum, near feeding predators—the role of reproductive requirements. Anim Behav 61:31–41CrossRefPubMedGoogle Scholar
  25. Seghers BH (1974) Schooling behaviour in the guppy Poecilia reticulata: an evolutionary response to predation. Evolution 28:486–489Google Scholar
  26. Sih A (1997) To hide or not to hide? Refuge use in a fluctuating environment. Trends Ecol Evol 12:375–376Google Scholar
  27. Sneddon LU (2003) The bold and the shy: individual differences in rainbow trout (Oncorhynchus mykiss). J Fish Biol 62:971–975Google Scholar
  28. Stein MB, Chartier MJ, Lizak MV, Jang L (2001) Familial aggregation of anxiety-related quantitative traits in generalized social phobia—clues to understanding “disorder” heritability? Am J Med Genet 105:79–83CrossRefPubMedGoogle Scholar
  29. Taborsky M (2001) The evolution of bourgeois, parasitic, and cooperative reproductive behaviors in fishes. J Hered 92:100–110PubMedGoogle Scholar
  30. Templeton JJ, Giraldeau LA (1996) Vicarious sampling: the use of personal and public information by starlings foraging in a simple patchy environment. Behav Ecol Sociobiol 38:105–114CrossRefGoogle Scholar
  31. Walsh RN, Cummins RA (1976) The open-field test: a critical review. Psychol Bull 83:482–504CrossRefGoogle Scholar
  32. Wilson DS (1998) Adaptive individual differences within single populations. Philos Trans R Soc Lond B Biol Sci 353:199–205CrossRefGoogle Scholar
  33. Wilson DS, Coleman K, Clark AB, Biederman L (1993) The shy-bold continuum in pumpkinseed sunfish (Lepomis gibbosus): an ecological study of a psychological trait. J Comp Psychol 107:250–260CrossRefGoogle Scholar
  34. Wilson DS, Clark AB, Coleman K, Dearstyne T (1994) Shyness and boldness in humans and other animals. Trends Ecol Evol 8:442–446CrossRefGoogle Scholar
  35. Wright D, Rimmer LB, Pritchard VL, Krause J, Butlin RK (2003) Inter- and intra-population variations in shoaling and boldness in the zebrafish (Danio rerio). Naturwissenschaften 90:374–377CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Ashley J. W. Ward
    • 1
    Email author
  • Philip Thomas
    • 2
  • Paul J. B. Hart
    • 1
  • Jens Krause
    • 2
  1. 1.Department of BiologyUniversity of LeicesterLeicesterUK
  2. 2.School of BiologyUniversity of LeedsLeedsUK

Personalised recommendations