Are some sharks more social than others? Short- and long-term consistencies in the social behavior of juvenile lemon sharks

  • J. S. FingerEmail author
  • T. L. Guttridge
  • A. D. M. Wilson
  • S. H. Gruber
  • J. Krause
Original Article


Despite substantial research interest in understanding individual-level consistency in behavioral attributes, significant knowledge gaps remain across traits and taxa. For example, relatively few studies have looked at social personality in large marine species such as elasmobranchs and whether or not individual differences in behavior are maintained in unstable social groups (i.e., fission-fusion dynamics). However, it is important to investigate this topic in other model species than the usually small species with short generation times typically investigated in these areas of behavioral ecology. Indeed, studies on ecologically diverse taxa could provide mechanistic insights into the emergence and maintenance of animal personality and dynamics of social groups in animals. In addition, understanding social behavior at the group- and individual-level could improve conservation management of these large animals with long generation times (e.g., removal of particular behavioral types by fisheries practices). Here, we investigated consistent individual differences in sociability in wild juvenile lemon sharks (Negaprion brevirostris) over both short- (4 to 18 days) and long-term (4 months) sampling periods. Individual sharks were observed in social groups and scored according to the number of social interactions performed during observations. Despite variable individual group compositions between repeated trials, sharks showed consistent individual differences in their social behavior over both time scales. These results suggest reduced plasticity and highlight individuality as an important explanatory variable for the social dynamics of juvenile lemon sharks. In addition, long-term stability observed in this wild population demonstrates the importance of personality in the daily behavioral repertoire of juvenile lemon sharks. Our results are discussed in the context of other shark studies and taxonomic groups and potential avenues for future research are proposed.

Significance statement

This study investigated the social personality axis in a wild population of juvenile lemon sharks. First, we demonstrated consistent individual differences in their tendency to socialize. Second, we showed that individuals maintained their differences over a four-month period in the wild. Finally, we found that individual social behaviors were maintained despite being tested in variable group compositions. These results highlight the importance of individuality in the social dynamic of a poorly investigated animal and suggest personality as an important aspect of juvenile lemon sharks’ everyday life over a relatively long-term period.


Fission-fusion Follower Group phenotype Leadership Personality Social dynamics 



We thank the volunteers and staff members of the Bimini Biological Field Station Foundation for their invaluable support. We are grateful to David Jacoby, Charlie Huveneers, and one anonymous referee for their comments on the manuscript, and Ralf Kurvers for his advice on the study design.

Funding information

This work was supported by the Elsa-Neumann-Stipendium des Landes Berlin, the Save Our Seas Foundation, the Guy Harvey Ocean Foundation, and the B-types project (SAW-2013-IGB-2) funded through the Leibniz Competition.

Compliance with ethical standards

Ethical statement

No sharks died during the experiments, and all were released at their site of capture with their color tags removed. Handling (e.g., size/sex determination and tagging) was performed within 5 min to minimize stress. All procedures were approved by the Department of Marine Resources, Bahamas (Permit no: MAF/LIA/22). No steps required anesthetizing the animals as this would increase handling time, increasing the stress on the animal.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable guidelines for the care and use of animals were followed.


  1. Aplin LM, Firth JA, Farine DR et al (2015) Consistent individual differences in the social phenotypes of wild great tits, Parus major. Anim Behav 108:117–127CrossRefPubMedCentralPubMedGoogle Scholar
  2. Archard GA, Braithwaite VA (2010) The importance of wild populations in studies of animal temperament. J Zool 281:149–160Google Scholar
  3. Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  4. Beleyur T, Bellur DU, Somanathan H (2015) Long-term behavioural consistency in prey capture but not in web maintenance in a social spider. Behav Ecol Sociobiol 69:1019–1028CrossRefGoogle Scholar
  5. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783CrossRefPubMedCentralPubMedGoogle Scholar
  6. Bergmuller R, Taborsky M (2010) Animal personality due to social niche specialisation. Trends Ecol Evol 25:504–511CrossRefPubMedGoogle Scholar
  7. Biro PA, Post JR (2008) Rapid depletion of genotypes with fast growth and bold personality traits from harvested fish populations. P Natl Acad Sci USA 105:2919–2922CrossRefGoogle Scholar
  8. Biro PA, Sampson P (2015) Fishing directly selects on growth rate via behaviour: implications of growth-selection that is independent of size. Proc R Soc B 282:20142283CrossRefPubMedGoogle Scholar
  9. Boulton K, Grimmer AJ, Rosenthal GG, Walling CA, Wilson AJ (2014) How stable are personalities? A multivariate view of behavioural variation over long and short timescales in the sheepshead swordtail, Xiphophorus birchmanni. Behav Ecol Sociobiol 68:791–803CrossRefGoogle Scholar
  10. Brown C, Irving E (2014) Individual personality traits influence group exploration in a feral guppy population. Behav Ecol 25:95–101CrossRefGoogle Scholar
  11. Brown CA, Gruber SH (1988) Age assessment of the lemon shark, Negaprion brevirostris, using tetracycline validated vertebral centra. Copeia 1988:747–753CrossRefGoogle Scholar
  12. Byrnes EE, Brown C (2016) Individual personality differences in port Jackson sharks Heterodontus portusjacksoni. J Fish Biol 89:1142–1157CrossRefPubMedGoogle Scholar
  13. Byrnes EE, Pouca CV, Brown C (2016a) Laterality strength is linked to stress reactivity in port Jackson sharks (Heterodontus portusjacksoni). Behav Brain Res 305:239–246CrossRefPubMedGoogle Scholar
  14. Byrnes EE, Pouca CV, Chambers SL, Brown C (2016b) Into the wild: developing field tests to examine the link between elasmobranch personality and laterality. Behaviour 153:1777–1793CrossRefGoogle Scholar
  15. Castanheira MF, Herrera M, Costas B, Conceicao LEC, Martins CIM (2013) Can we predict personality in fish? Searching for consistency over time and across contexts. PLoS One 8:e62037CrossRefPubMedCentralPubMedGoogle Scholar
  16. Castanheira MF, Paramo SM, Figueiredo F, Cerqueira M, Millot S, Oliveira CCV, Martins CIM, Conceicao LEC (2016) Are coping styles consistent in the teleost fish Sparus aurata through sexual maturation and sex reversal? Fish Physiol Biochem 42:1441–1452CrossRefPubMedGoogle Scholar
  17. Chapman DD, Babcock EA, Gruber SH, Dibattista JD, Franks BR, Kessel SA, Guttridge T, Pikitch EK, Feldheim KA (2009) Long-term natal site-fidelity by immature lemon sharks (Negaprion brevirostris) at a subtropical island. Mol Ecol 18:3500–3507CrossRefPubMedGoogle Scholar
  18. Conrad JL, Weinersmith KL, Brodin T, Saltz JB, Sih A (2011) Behavioural syndromes in fishes: a review with implications for ecology and fisheries management. J Fish Biol 78:395–435CrossRefPubMedGoogle Scholar
  19. Cote J, Clobert J (2007) Social personalities influence natal dispersal in a lizard. Proc R Soc Lond B 274:383–390CrossRefGoogle Scholar
  20. Cote J, Fogarty S, Sih A (2012) Individual sociability and choosiness between shoal types. Anim Behav 83:1469–1476CrossRefGoogle Scholar
  21. Croft DP, Madden JR, Franks DW, James R (2011) Hypothesis testing in animal social networks. Trends Ecol Evol 26:502–507CrossRefPubMedGoogle Scholar
  22. 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
  23. Debeffe L, Lemaitre JF, Bergvall UA et al (2015) Short- and long-term repeatability of docility in the roe deer: sex and age matter. Anim Behav 109:53–63CrossRefGoogle Scholar
  24. Dibattista JD, Feldheim KA, Gruber SH, Hendry AP (2007) When bigger is not better: selection against large size, high condition and fast growth in juvenile lemon sharks. J Evol Biol 20:201–212CrossRefPubMedGoogle Scholar
  25. Dingemanse NJ, Wolf M (2010) Recent models for adaptive personality differences: a review. Philos T Roy Soc B 365:3947–3958CrossRefGoogle Scholar
  26. Dulvy NK, Fowler SL, Musick JA et al (2014) Extinction risk and conservation of the world’s sharks and rays. elife 3:e00590CrossRefPubMedCentralPubMedGoogle Scholar
  27. Estes JA, Terborgh J, Brashares JS et al (2011) Trophic downgrading of planet earth. Science 333:301–306CrossRefPubMedGoogle Scholar
  28. Farine DR, Montiglio PO, Spiegel O (2015) From individuals to groups and back: the evolutionary implications of group phenotypic composition. Trends Ecol Evol 30:609–621CrossRefPubMedCentralPubMedGoogle Scholar
  29. Finger JS, Dhellemmes F, Guttridge TL (2017) Personality in elasmobranchs with a focus on sharks: early evidence, challenges, and future directions. In: Vonk J, Weiss A, Kuczaj SA (eds) Personality in nonhuman animals. Springer, Berlin, pp 129–152CrossRefGoogle Scholar
  30. Finger JS, Dhellemmes F, Guttridge TL, Kurvers R, Gruber SH, Krause J (2016) Rate of movement of juvenile lemon sharks in a novel open field, are we measuring activity or reaction to novelty? Anim Behav 116:75–82CrossRefGoogle Scholar
  31. Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psychol Bull 127:45–86CrossRefPubMedGoogle Scholar
  32. Gruber SH, de Marignac JRC, Hoenig JM (2001) Survival of juvenile lemon sharks at Bimini, Bahamas, estimated by mark-depletion experiments. Trans Am Fish Soc 130:376–384CrossRefGoogle Scholar
  33. Guttridge TL, Gruber SH, DiBattista JD, Feldheim KA, Croft DP, Krause S, Krause J (2011) Assortative interactions and leadership in a free-ranging population of juvenile lemon shark Negaprion brevirostris. Mar Ecol-Prog Ser 423:235–245CrossRefGoogle Scholar
  34. Guttridge TL, Gruber SH, Gledhill KS, Croft DP, Sims DW, Krause J (2009) Social preferences of juvenile lemon sharks, Negaprion brevirostris. Anim Behav 78:543–548CrossRefGoogle Scholar
  35. Harcourt JL, Ang TZ, Sweetman G, Johnstone RA, Manica A (2009a) Social feedback and the emergence of leaders and followers. Curr Biol 19:248–252CrossRefPubMedGoogle Scholar
  36. Harcourt JL, Sweetman G, Johnstone RA, Manica A (2009b) Personality counts: the effect of boldness on shoal choice in three-spined sticklebacks. Anim Behav 77:1501–1505CrossRefGoogle Scholar
  37. Huveneers C, Rogers PJ, Beckmann C, Semmens JM, Bruce BD, Seuront L (2013) The effects of cage-diving activities on the fine-scale swimming behaviour and space use of white sharks. Mar Biol 160:2863–2875CrossRefGoogle Scholar
  38. Jacoby DMP, Croft DP, Sims DW (2012a) Social behaviour in sharks and rays: analysis, patterns and implications for conservation. Fish Fish 13:399–417CrossRefGoogle Scholar
  39. Jacoby DMP, Fear LN, Sims DW, Croft DP (2014) Shark personalities? Repeatability of social network traits in a widely distributed predatory fish. Behav Ecol Sociobiol 68:1995–2003CrossRefGoogle Scholar
  40. Jacoby DMP, Sims DW, Croft DP (2012b) The effect of familiarity on aggregation and social behaviour in juvenile small spotted catsharks Scyliorhinus canicula. J Fish Biol 81:1596–1610CrossRefPubMedGoogle Scholar
  41. Johnstone RA, Manica A (2011) Evolution of personality differences in leadership. P Natl Acad Sci USA 108:8373–8378CrossRefGoogle Scholar
  42. Keller BA, Finger JS, Gruber SH, Abel DC, Guttridge TL (2017) The effects of familiarity on the social interactions of juvenile lemon sharks, Negaprion brevirostris. J Exp Mar Biol Ecol 489:24–31CrossRefGoogle Scholar
  43. King AJ, Furtbauer I, Mamuneas D, James C, Manica A (2013) Sex-differences and temporal consistency in stickleback fish boldness. PLoS One 8:e81116CrossRefPubMedCentralPubMedGoogle Scholar
  44. Klimley AP (1985) Schooling in Sphyrna lewini, a species with low risk of predation: a non-egalitarian state. Z Tierpsychol 70:297–319CrossRefGoogle Scholar
  45. Koski SE (2011) Social personality traits in chimpanzees: temporal stability and structure of behaviourally assessed personality traits in three captive populations. Behav Ecol Sociobiol 65:2161–2174CrossRefGoogle Scholar
  46. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, OxfordGoogle Scholar
  47. Kurvers R, Eijkelenkamp B, van Oers K, van Lith B, van Wieren SE, Ydenberg RC, Prins HHT (2009) Personality differences explain leadership in barnacle geese. Anim Behav 78:447–453CrossRefGoogle Scholar
  48. Laskowski KL, Bell AM (2014) Strong personalities, not social niches, drive individual differences in social behaviours in sticklebacks. Anim Behav 90:287–295CrossRefPubMedCentralPubMedGoogle Scholar
  49. Lewison RL, Crowder LB, Read AJ, Freeman SA (2004) Understanding impacts of fisheries bycatch on marine megafauna. Trends Ecol Evol 19:598–604CrossRefGoogle Scholar
  50. Magnhagen C (2012) Personalities in a crowd: what shapes the behaviour of Eurasian perch and other shoaling fishes? Curr Zool 58:35–44CrossRefGoogle Scholar
  51. Magnhagen C, Bunnefeld N (2009) Express your personality or go along with the group: what determines the behaviour of shoaling perch? Proc R Soc Lond B 276:3369–3375CrossRefGoogle Scholar
  52. Magnhagen C, Staffan F (2005) Is boldness affected by group composition in young-of-the-year perch (Perca fluviatilis)? Behav Ecol Sociobiol 57:295–303CrossRefGoogle Scholar
  53. Manire CA, Gruber SH (1991) Effect of M-type DART tags on field growth of juvenile lemon sharks. Trans Am Fish Soc 120:776–780CrossRefGoogle Scholar
  54. Matich P, Heithaus MR (2015) Individual variation in ontogenetic niche shifts in habitat use and movement patterns of a large estuarine predator (Carcharhinus leucas). Oecologia 178:347–359CrossRefPubMedGoogle Scholar
  55. Meijering E, Dzyubachyk O, Smal I (2012) Methods for cell and particle tracking. Methods Enzymol 504:183–200CrossRefPubMedGoogle Scholar
  56. Mittelbach GG, Ballew NG, Kjelvik MK (2014) Fish behavioral types and their ecological consequences. Can J Fish Aquat Sci 71:927–944CrossRefGoogle Scholar
  57. Morrissey JF, Gruber SH (1993) Home range of juvenile lemon sharks, Negaprion brevirostris. Copeia 1993:425–434CrossRefGoogle Scholar
  58. Mourier J, Bass NC, Guttridge TL, Day J, Brown C (2017) Does detection range matter for inferring social networks in a benthic shark using acoustic telemetry? Royal Soc Open Sci 4:170485CrossRefGoogle Scholar
  59. Mourier J, Vercelloni J, Planes S (2012) Evidence of social communities in a spatially structured network of a free-ranging shark species. Anim Behav 83:389–401CrossRefGoogle Scholar
  60. Mucientes GR, Queiroz N, Sousa LL, Tarroso P, Sims DW (2009) Sexual segregation of pelagic sharks and the potential threat from fisheries. Biol Lett 5:156–159CrossRefPubMedCentralPubMedGoogle Scholar
  61. Myrberg AA, Gruber SH (1974) The behavior of the bonnethead shark, Sphyrna tiburo. Copeia 1974:358–374CrossRefGoogle Scholar
  62. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956PubMedGoogle Scholar
  63. Nakayama S, Stumpe MC, Manica A, Johnstone RA (2013) Experience overrides personality differences in the tendency to follow but not in the tendency to lead. Proc R Soc B 280:20131724CrossRefPubMedGoogle Scholar
  64. Northcutt RG (1977) Elasmobranch central nervous system organization and its possible evolutionary significance. Am Zool 17:411–429CrossRefGoogle Scholar
  65. 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
  66. Rasband W (1997) ImageJ. US National Institutes of Health, BethesdaGoogle Scholar
  67. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318CrossRefPubMedGoogle Scholar
  68. R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  69. Scheipl F, Greven S, Kuchenhoff H (2008) Size and power of tests for a zero random effect variance or polynomial regression in additive and linear mixed models. Comput Stat Data Anal 52:3283–3299CrossRefGoogle Scholar
  70. Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Q Rev Biol 79:241–277CrossRefPubMedGoogle Scholar
  71. Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289CrossRefPubMedGoogle Scholar
  72. Stamps J, Groothuis TGG (2010) The development of animal personality: relevance, concepts and perspectives. Biol Rev 85:301–325CrossRefPubMedGoogle Scholar
  73. Stamps JA (2007) Growth-mortality tradeoffs and ‘personality traits’ in animals. Ecol Lett 10:355–363CrossRefPubMedGoogle Scholar
  74. Stevens JD, Bonfil R, Dulvy NK, Walker PA (2000) The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES J Mar Sci 57:476–494CrossRefGoogle Scholar
  75. Sutter DAH, Suski CD, Philipp DP, Klefoth T, Wahl DH, Kersten P, Cooke SJ, Arlinghaus R (2012) Recreational fishing selectively captures individuals with the highest fitness potential. P Natl Acad Sci USA 109:20960–20965CrossRefGoogle Scholar
  76. Towner AV, Leos-Barajas V, Langrock R, Schick RS, Smale MJ, Kaschke T, Jewell OJD, Papastamatiou YP (2016) Sex-specific and individual preferences for hunting strategies in white sharks. Funct Ecol 30:1397–1407CrossRefGoogle Scholar
  77. Vaudo JJ, Wetherbee BM, Harvey G, Nemeth RS, Aming C, Burnie N, Howey-Jordan LA, Shivji MS (2014) Intraspecific variation in vertical habitat use by tiger sharks (Galeocerdo cuvier) in the western North Atlantic. Ecol Evol 4:1768–1786CrossRefPubMedCentralPubMedGoogle Scholar
  78. Vrtelova J, Ferrari MCO, Manek AK, Chivers DP (2016) Consistent long-term behavioural traits are linked to morphological defences in common carp (Cyprinus carpio). Behaviour 153:15–30CrossRefGoogle Scholar
  79. Webster MM, Ward AJW (2011) Personality and social context. Biol Rev 86:759–773CrossRefPubMedGoogle Scholar
  80. Wilson ADM, Brownscombe JW, Krause J, Krause S, Gutowsky LFG, Brooks EJ, Cooke SJ (2015) Integrating network analysis, sensor tags, and observation to understand shark ecology and behavior. Behav Ecol 26:1577–1586CrossRefGoogle Scholar
  81. Wilson ADM, Krause S, James R, Croft DP, Ramnarine IW, Borner KK, Clement RJG, Krause J (2014) Dynamic social networks in guppies (Poecilia reticulata). Behav Ecol Sociobiol 68:915–925CrossRefGoogle Scholar
  82. Wolf M, Krause J (2014) Why personality differences matter for social functioning and social structure. Trends Ecol Evol 29:306–308CrossRefPubMedGoogle Scholar
  83. Wolf M, van Doorn GS, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–584CrossRefPubMedGoogle Scholar
  84. Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27:452–461CrossRefPubMedGoogle Scholar
  85. Wuerz Y, Krüger O (2015) Personality over ontogeny in zebra finches: long-term repeatable traits but unstable behavioural syndromes. Front Zool 12:S9CrossRefPubMedCentralPubMedGoogle Scholar
  86. Yopak KE, Lisney TJ, Collin SP, Montgomery JC (2007) Variation in brain organization and cerebellar foliation in chondrichthyans: sharks and holocephalans. Brain Behav Evol 69:280–300CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Faculty of Life Sciences, Albrecht Daniel Thaer-InstitutHumboldt-Universität zu BerlinBerlinGermany
  2. 2.Bimini Biological Field Station FoundationSouth BiminiBahamas
  3. 3.Leibniz-Institute of Freshwater Ecology and Inland FisheriesBerlinGermany
  4. 4.School of Life and Environmental SciencesUniversity of SydneySydneyAustralia

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