Consistent Individual Differences Drive Collective Behavior and Group Functioning of Schooling Fish

Abstract

The ubiquity of consistent inter-individual differences in behavior ("animal personalities") [1, 2] suggests that they might play a fundamental role in driving the movements and functioning of animal groups [3, 4], including their collective decision-making, foraging performance, and predator avoidance. Despite increasing evidence that highlights their importance [5-16], we still lack a unified mechanistic framework to explain and to predict how consistent inter-individual differences may drive collective behavior. Here we investigate how the structure, leadership, movement dynamics, and foraging performance of groups can emerge from inter-individual differences by high-resolution tracking of known behavioral types in free-swimming stickleback (Gasterosteus aculeatus) shoals. We show that individual's propensity to stay near others, measured by a classic "sociability" assay, was negatively linked to swim speed across a range of contexts, and predicted spatial positioning and leadership within groups as well as differences in structure and movement dynamics between groups. In turn, this trait, together with individual's exploratory tendency, measured by a classic "boldness" assay, explained individual and group foraging performance. These effects of consistent individual differences on group-level states emerged naturally from a generic model of self-organizing groups composed of individuals differing in speed and goal-orientedness. Our study provides experimental and theoretical evidence for a simple mechanism to explain the emergence of collective behavior from consistent individual differences, including variation in the structure, leadership, movement dynamics, and functional capabilities of groups, across social and ecological scales. In addition, we demonstrate individual performance is conditional on group composition, indicating how social selection may drive behavioral differentiation between individuals.

References 46

1. 1.

   Réale D., Reader S.M., Sol D., McDougall P.T., Dingemanse N.J. Integrating animal temperament within ecology and evolution. Biol. Rev. Camb. Philos. Soc. 2007;82:291-318.

   Not in our library10.1111/j.1469-185x.2007.00010.x

2. 2.

   Bell A.M., Hankison S.J., Laskowski K.L. The repeatability of behaviour: a meta-analysis. Anim. Behav. 2009;77:771-783.

   Not in our library10.1016/j.anbehav.2008.12.022

3. 3.

   Webster M.M., Ward A.J.W. Personality and social context. Biol. Rev. Camb. Philos. Soc. 2011;86:759-773.

   Not in our library10.1111/j.1469-185x.2010.00169.x

4. 4.

   Wolf M., Krause J. Why personality differences matter for social functioning and social structure. Trends Ecol. Evol. 2014;29:306-308.

   Not in our library10.1016/j.tree.2014.03.008

5. 5.

   Ward A.J.W., Thomas P., Hart P.J.B., Krause J. Correlates of boldness in three-spined sticklebacks (Gasterosteus aculeatus). Behav. Ecol. Sociobiol. 2004;55:561-568.

   Not in our library

6. 6.

   Kurvers R.H.J.M., Eijkelenkamp B., van Oers K., van Lith B., van Wieren S.E., Ydenberg R.C., Prins H.H.T. Personality differences explain leadership in barnacle geese. Anim. Behav. 2009;78:447-453.

   Not in our library

7. 7.

   Harcourt J.L., Ang T.Z., Sweetman G., Johnstone R.A., Manica A. Social feedback and the emergence of leaders and followers. Curr. Biol. 2009;19:248-252.

   Not in our library10.1016/j.cub.2008.12.051

8. 8.

   Pettit B., Ákos Z., Vicsek T., Biro D. Speed determines leadership and leadership determines learning during pigeon flocking. Curr. Biol. 2015;25:3132-3137.

   Not in our library10.1016/j.cub.2015.10.044

9. 9.

   Pike T.W., Samanta M., Lindström J., Royle N.J. Behavioural phenotype affects social interactions in an animal network. Proc. Biol. Sci. 2008;275:2515-2520.

   Not in our library10.1098/rspb.2008.0744

10. 10.

    Aplin L.M., Farine D.R., Morand-Ferron J., Cole E.F., Cockburn A., Sheldon B.C. Individual personalities predict social behaviour in wild networks of great tits (Parus major). Ecol. Lett. 2013;16:1365-1372.

    Not in our library10.1111/ele.12181

11. 11.

    Jolles J.W., Fleetwood-Wilson A., Nakayama S., Stumpe M.C., Johnstone R.A., Manica A. The role of social attraction and its link with boldness in the collective movements of three-spined sticklebacks. Anim. Behav. 2015;99:147-153.

    Not in our library10.1016/j.anbehav.2014.11.004

12. 12.

    Farine D.R., Strandburg-Peshkin A., Couzin I.D., Berger-Wolf T.Y., Crofoot M.C. Individual variation in local interaction rules can explain emergent patterns of spatial organization in wild baboons. Proc. Biol. Sci. 2017;284:25-29.

    Not in our library10.1098/rspb.2016.2243

13. 13.

    Dyer J.R.G., Croft D.P., Morrell L.J., Krause J. Shoal composition determines foraging success in the guppy. Behav. Ecol. 2009;20:165-171.

    Not in our library

14. 14.

    Laskowski K.L., Montiglio P.O., Pruitt J.N. Individual and group performance suffers from social niche disruption. Am. Nat. 2016;187:776-785.

    Not in our library10.1086/686220

15. 15.

    Pruitt J.N., Riechert S.E. How within-group behavioural variation and task efficiency enhance fitness in a social group. Proc. Biol. Sci. 2011;278:1209-1215.

    Not in our library10.1098/rspb.2010.1700

16. 16.

    Ioannou C.C., Dall S.R.X. Individuals that are consistent in risk-taking benefit during collective foraging. Sci. Rep. 2016;6:33991.

    Not in our library10.1038/srep33991

17. 17.

    Smith B.R., Blumstein D.T. Fitness consequences of personality: a meta-analysis. Behav. Ecol. 2008;19:448-455.

    Not in our library

18. 18.

    Sih A., Cote J., Evans M., Fogarty S., Pruitt J. Ecological implications of behavioural syndromes. Ecol. Lett. 2012;15:278-289.

    Not in our library10.1111/j.1461-0248.2011.01731.x

19. 19.

    Réale D., Dingemanse N.J., Kazem A.J.N., Wright J. Evolutionary and ecological approaches to the study of personality. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010;365:3937-3946.

    Not in our library10.1098/rstb.2010.0222

20. 20.

    Schaerf, T.M., Herbert-Read, J.E., Myerscough, M.R., Sumpter, D.J.T., and Ward, A.J.W. (2016). Identifying differences in the rules of interaction between individuals in moving animal groups. arXiv, arXiv:1601.08202, http://arxiv.org/abs/1601.08202.

    Not in our library10.1098/rsif.2020.0925

21. 21.

    Couzin I.D., Krause J. Self-organization and collective behavior in vertebrates. Adv. Stud. Behav. 2003;32:1-75.

    Not in our library

22. 22.

    Sumpter D.J.T. Collective Animal Behavior. 2010.

    Not in our library

23. 23.
    Understanding how animal groups achieve coordinated movement · 2016

    No notice
24. 24.

    Couzin I.D., Krause J., James R., Ruxton G.D., Franks N.R. Collective memory and spatial sorting in animal groups. J. Theor. Biol. 2002;218:1-11.

    Not in our library10.1006/jtbi.2002.3065

25. 25.
    Collective States, Multistability and Transitional Behavior in Schooling Fish · 2013

    No notice
26. 26.

    Couzin I.D., Krause J., Franks N.R., Levin S.A. Effective leadership and decision-making in animal groups on the move. Nature. 2005;433:513-516.

    Not in our library10.1038/nature03236

27. 27.

    Ioannou C.C., Singh M., Couzin I.D. Potential leaders trade off goal-oriented and socially oriented behavior in mobile animal groups. Am. Nat. 2015;186:284-293.

    Not in our library10.1086/681988

28. 28.

    Persson L., Eklöv P. Prey refuges affecting interactions between piscivorous perch and juvenile perch and roach. Ecology. 1995;76:70-81.

    Not in our library

29. 29.

    Jolles J.W., Manica A., Boogert N.J. Food intake rates of inactive fish are positively linked to boldness in three-spined sticklebacks Gasterosteus aculeatus. J. Fish Biol. 2016;88:1661-1668.

    Not in our library10.1111/jfb.12934

30. 30.

    Krause J., Ruxton G.D. Living in Groups. 2002.

    Not in our library

31. 31.

    Ward A., Webster M. Sociality: The Behaviour of Group-Living Animals. 2016.

    Not in our library

32. 32.

    Katz Y., Tunstrøm K., Ioannou C.C., Huepe C., Couzin I.D. Inferring the structure and dynamics of interactions in schooling fish. Proc. Natl. Acad. Sci. USA. 2011;108:18720-18725.

    Not in our library10.1073/pnas.1107583108

33. 33.

    Herbert-Read J.E., Perna A., Mann R.P., Schaerf T.M., Sumpter D.J.T., Ward A.J.W. Inferring the rules of interaction of shoaling fish. Proc. Natl. Acad. Sci. USA. 2011;108:18726-18731.

    Not in our library10.1073/pnas.1109355108

34. 34.

    Herbert-Read J.E., Krause S., Morrell L.J., Schaerf T.M., Krause J., Ward A.J.W. The role of individuality in collective group movement. Proc. Biol. Sci. 2012;280:20122564.

    Not in our library10.1098/rspb.2012.2564

35. 35.

    Nagy M., Akos Z., Biro D., Vicsek T. Hierarchical group dynamics in pigeon flocks. Nature. 2010;464:890-893.

    Not in our library10.1038/nature08891

36. 36.

    Johnstone R.A., Manica A. Evolution of personality differences in leadership. Proc. Natl. Acad. Sci. USA. 2011;108:8373-8378.

    Not in our library10.1073/pnas.1102191108

37. 37.
    From Individuals to Groups and Back: The Evolutionary Implications of Group Phenotypic Composition · 2015

    No notice
38. 38.

    Spiegel O., Leu S.T., Bull C.M., Sih A. What’s your move? Movement as a link between personality and spatial dynamics in animal populations. Ecol. Lett. 2017;20:3-18.

    Not in our library10.1111/ele.12708

39. 39.

    Borg B., Bornestaf C., Hellqvist A., Schmitz M., Mayer I. Mechanisms in the photoperiodic control of reproduction in the stickleback. Behav. 2004;141:1521-1530.

    Not in our library

40. 40.

    Jolles J.W., Aaron Taylor B., Manica A. Recent social conditions affect boldness repeatability in individual sticklebacks. Anim. Behav. 2016;112:139-145.

    Not in our library10.1016/j.anbehav.2015.12.010

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