Behavioral Ecology and Sociobiology

, Volume 64, Issue 4, pp 693–702 | Cite as

Are behavioral syndromes invariant? Spatiotemporal variation in shy/bold behavior in squid

  • David L. SinnEmail author
  • Natalie A. Moltschaniwskyj
  • Erik Wapstra
  • Sasha R. X. Dall
Original Paper


Behavioral syndromes are correlated suites of behavior, analogous to human personality traits. Most work to date has been taken from limited “snapshots” in space and time, with the implicit assumption that a behavioral syndrome is an invariant property, fixed by evolutionary constraints or adaptations. However, directional selection on two mechanistically independent traits (selective covariance) could also result in correlated behaviors. Previously, we have shown that shy/bold behavior in Southern dumpling squid (Euprymna tasmanica) across predator encounter and feeding risk contexts is genetically and phenotypically uncoupled, and hence potentially free to vary independently. Here, we collected data on shy/bold behaviors from two independent wild populations of squid in two different years to test whether behavioral correlations across these same two functional contexts vary through time and space. We detected significant influences of population, sex, and body size on the expression of boldness in squid within each functional context, and this was coupled with significant differences in relative population density and adult sex ratio. Despite these changes in behavior and demographic parameters, we found that correlations between boldness scores across the two functional contexts were largely absent in both wild populations of squid in both years. Our work suggests that some animal groups may be largely characterized by context-specific behavioral expression. A theoretical framework which conceptualizes behavioral syndromes resulting from context-specific behavioral rules may be needed to fully understand why behaviors are sometimes correlated, and why sometimes they are not.


Behavioral syndromes Shy/bold Selective covariance State-dependent optimization 



This work was conducted in partial fulfillment of the requirements for D.L. Sinn's PhD degree at the University of Tasmania. Funding was provided by a Holsworth Wildlife Research Fund grant (M0013237) and Australian International Postgraduate Research scholarship to DLS. Tom Fox-Smith, Jonothan Newman, and Colin Johnson provided essential logistical support in the field. Kees van Oers, Piet Drent, and Luc Alain-Giraldeau provided helpful discussions; Alison Bell, Jo McEvoy, and two anonymous reviewers gave constructive criticism on earlier drafts that greatly improved the final version. Experimental methods for all squid conformed to Australian law and the standards set by the University of Tasmania Animal Ethics Committee (2003).


  1. Alvarez D, Bell AM (2007) Sticklebacks from streams are more bold than sticklebacks from ponds. Behav Processes 76:215–217CrossRefPubMedGoogle Scholar
  2. Armbruster WS, Schwaegerle KE (1996) Causes of covariation of phenotypic traits among populations. J Evol Biol 9:261–276CrossRefGoogle Scholar
  3. Bell AM (2005) Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J Evol Biol 18:464–473CrossRefPubMedGoogle Scholar
  4. Bell AM (2007) Future directions in behavioural syndromes research. Proc R Soc Biol Sci Ser B 274:755–761CrossRefGoogle Scholar
  5. Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834CrossRefPubMedGoogle Scholar
  6. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57:289–300Google Scholar
  7. Boal JG, Hylton RA, Gonzalez SA, Hanlon RT (1999) Effects of crowding on the social behavior of cuttlefish (Sepia officinalis). Contemp Top Lab Anim Sci 38:49–55Google Scholar
  8. Both C, Dingemanse NJ, Drent PJ, Tinbergen JM (2005) Pairs of extreme avian personalities have highest reproductive success. J Anim Ecol 74:667–674CrossRefGoogle Scholar
  9. Boyle PR, Boletzky Sv (1996) Cephalopod populations: definition and dynamics. Philos T Roy Soc B 351:985–1002CrossRefGoogle Scholar
  10. Brydges NM, Colegrave N, Heathcote RJP, Braithwaite VA (2008) Habitat stability and predation pressure affect temperament behaviours in populations of three-spined sticklebacks. J Anim Ecol 77:229–235CrossRefPubMedGoogle Scholar
  11. Cheverud JM (1984) Quantitative genetics and developmental constraints on evolution by natural selection. J Theor Biol 110:155–172CrossRefPubMedGoogle Scholar
  12. Coleman K, Wilson DS (1998) Shyness and boldness in pumpkinseed sunfish: individual differences are context-specific. Anim Behav 56:927–936CrossRefPubMedGoogle Scholar
  13. Dall SRX, Houston AI, McNamara JM (2004) The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett 7:734–739CrossRefGoogle Scholar
  14. Dingemanse NJ, Réale D (2005) Natural selection and animal personality. Behaviour 142:1159–1184CrossRefGoogle Scholar
  15. Dingemanse NJ, Wright J, Kazem AJN, Thomas DK, Hickling R, Dawnay N (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76:1128–1138CrossRefPubMedGoogle Scholar
  16. Duckworth RA (2006) Behavioral correlations across breeding contexts provide a mechanism for a cost of aggression. Behav Ecol 17:1011–1019CrossRefGoogle Scholar
  17. Endler JA (1986) Natural selection in the wild. Princeton University Press, PrincetonGoogle Scholar
  18. Epstein S (1983) Aggregation and beyond: some basic issues on the prediction of behavior. J Personal 51:360–392CrossRefGoogle Scholar
  19. Fleeson W (2004) Moving personality beyond the person-situation debate. Curr Dir Psychol Sci 13:83–87CrossRefGoogle Scholar
  20. Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psychol Bull 127:45–86CrossRefPubMedGoogle Scholar
  21. Hanlon RT (1996) Evolutionary games that squids play: fighting, courting, sneaking, and mating behaviors used for sexual selection in Loligo pealei. Biol Bull 191:309–310Google Scholar
  22. Heithaus MR, Frid A, Wirsing AJ, Dill LM, Fourqurean JW, Burkholder D, Thomson J, Bejder L (2007) State-dependent risk-taking by green sea turtles mediates top-down effects of tiger shark intimidation in a marine ecosystem. J Anim Ecol 76:837–844CrossRefPubMedGoogle Scholar
  23. Huntingford FA (1976) The relationship between anti-predator behaviour and aggression among conspecifics in the three-spined stickleback. Anim Behav 24:245–260CrossRefGoogle Scholar
  24. Huntingford FA (1982) Do inter- and intraspecific aggression vary in relation to predation pressure in sticklebacks? Anim Behav 30:909–916CrossRefGoogle Scholar
  25. Hutchinson JMC, Gigerenzer G (2005) Simple heuristics and rules of thumb: where psychologists and behavioural biologists might meet. Behav Processes 69:97–124CrossRefPubMedGoogle Scholar
  26. Johnson JC, Sih A (2005) Precopulatory sexual cannibalism in fishing spiders (Dolomedes triton): a role for behavioural syndromes. Behav Ecol Sociobiol 58:390–396CrossRefGoogle Scholar
  27. Kimbell JR, McFall-Ngai MJ, Roderick GK (2002) Two genetically distinct populations of bobtail squid, Euprymna scolopes, exist on the island of O'ahu. Pac Sci 56:347–355CrossRefGoogle Scholar
  28. Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226CrossRefGoogle Scholar
  29. Magnhagen C (2007) Social influence on the correlation between behaviours in young-of-the-year perch. Behav Ecol Sociobiol 61:525–531CrossRefGoogle Scholar
  30. Maxwell MR, Hanlon RT (2000) Female reproductive output in the squid Loligo pealeii: multiple egg clutches and implications for a spawning strategy. Mar Ecol Prog Ser 199:159–170CrossRefGoogle Scholar
  31. McNamara JM, Gasson CE, Houston AI (1999) Incorporating rules for responding into evolutionary games. Nature 401:368–371PubMedGoogle Scholar
  32. Messenger JB (1977) Prey-capture and learning in the cuttlefish, Sepia. Symp Zool Soc Lond 38:347–376Google Scholar
  33. Mougeot F, Redpath SM, Leckie F, Hudson PJ (2003) The effect of aggressiveness on the population dynamics of a territorial bird. Nature 421:737–739CrossRefPubMedGoogle Scholar
  34. Naud MJ, Hanlon RT, Hall KC, Shaw PW, Havenhand JN (2004) Behavioral and genetic assessment of reproductive success in a spawning aggregation of the Australian giant cuttlefish, Sepia apama. Anim Behav 67:1043–1050CrossRefGoogle Scholar
  35. Norman M, Reid A (2000) A guide to squid, cuttlefish, and octopuses of Australasia. The Gould League and CSIRO Publishing, CollingwoodGoogle Scholar
  36. Packard A (1972) Cephalopods and fish: the limits of convergence. Biol Rev 47:241–307CrossRefGoogle Scholar
  37. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeGoogle Scholar
  38. Rands SA, Cowlishaw G, Pettifor RA, Rowcliffe JM, Johnstone RA (2003) Spontaneous emergence of leaders and followers in foraging pairs. Nature 423:432–434CrossRefPubMedGoogle Scholar
  39. Rankin DJ, Kokko H (2007) Do males matter? The role of males in population dynamics. Oikos 116:335–348CrossRefGoogle Scholar
  40. Réale D, Festa-Bianchet M (2003) Predator-induced natural selection on temperament in bighorn ewes. Anim Behav 65:463–470CrossRefGoogle Scholar
  41. Réale D, Reader SM, Sol D, Mcdougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:1–28CrossRefGoogle Scholar
  42. Sih A, Watters JV (2005) The mix matters: behavioural types and group dynamics in water striders. Behaviour 142:1417–1431CrossRefGoogle Scholar
  43. Sih A, Bell A, Johnson JC (2004a) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:373–378Google Scholar
  44. Sih A, Bell AM, Johnson JC, Ziemba RE (2004b) Behavioral syndromes: an integrative overview. Q Rev Biol 79:242–277CrossRefGoogle Scholar
  45. Sinn DL, Moltschaniwskyj NA (2005) Personality traits in dumpling squid (Euprymna tasmanica): context-specific traits and their correlation with biological characteristics. J Comp Psychol 119:99–110CrossRefPubMedGoogle Scholar
  46. Sinn DL, Apiolaza LA, Moltschaniwskyj NA (2006) Heritability and fitness-related consequences of squid personality traits. J Evol Biol 19:1437–1447CrossRefPubMedGoogle Scholar
  47. Sinn DL, Gosling SD, Moltschaniwskyj NA (2008) Development of shy/bold behaviour in squid: context-specific phenotypes associated with developmental plasticity. Anim Behav 75:433–442CrossRefGoogle Scholar
  48. Stamps JA (2007) Growth-mortality tradeoffs and ‘personality traits’ in animals. Ecol Lett 10:355–363CrossRefPubMedGoogle Scholar
  49. Stapley J, Keogh JS (2005) Behavioral syndromes influence mating systems: floater pairs of a lizard have heavier offspring. Behav Ecol 16:514–520CrossRefGoogle Scholar
  50. Tabachnick BG, Fidell LS (1996) Using multivariate statistics, 3rd edn. HarperCollins, New YorkGoogle Scholar
  51. van Oers K, Klunder M, Drent PJ (2005) Context dependence of personalities: risk-taking behavior in a social and a nonsocial situation. Behav Ecol 16:716–723CrossRefGoogle Scholar
  52. West-Eberhard MJ (1979) Sexual selection, social competition, and evolution. Proc Am Philos Soc 123:222–234Google Scholar
  53. Wilson DS (1998) Adaptive individual differences within single populations. Philos T Roy Soc B 353:199–205CrossRefGoogle Scholar
  54. Wilson DS, Clark AB, Coleman K, Dearstyne T (1994) Shyness and boldness in humans and other animals. Trends Ecol Evol 9:442–446Google Scholar
  55. Wolf M, Sander van Doorn S, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–585CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • David L. Sinn
    • 1
    • 2
    • 3
    Email author
  • Natalie A. Moltschaniwskyj
    • 1
  • Erik Wapstra
    • 3
  • Sasha R. X. Dall
    • 4
  1. 1.School of AquacultureUniversity of TasmaniaLauncestonTasmania
  2. 2.School of Plant ScienceUniversity of TasmaniaHobartTasmania
  3. 3.School of ZoologyUniversity of TasmaniaHobartAustralia
  4. 4.Centre for Ecology & Conservation, School of BiosciencesUniversity of Exeter, Cornwall CampusPenrynUK

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