Environmental Biology of Fishes

, Volume 80, Issue 1, pp 91–101 | Cite as

The effects of early and adult social environment on zebrafish (Danio rerio) behavior

  • Jason A. MoretzEmail author
  • Emília P. Martins
  • Barrie D. Robison
Original paper


Because early social experience can have a profound effect on later mate and social choices, the availability of options and decisions made early in development can have major effects on adult behavior. Herein, we use strain differences among zebrafish, Danio rerio, as an experimental tool to test the effects of social experience on behavior. By manipulating the strain composition of groups in which the subject fish are housed at different ages, we tested (1) whether mixing with dissimilar individuals influenced subsequent behavior, (2) whether prolonged mixing during the juvenile stage had a more pronounced effect than a shorter period of mixing during adulthood and (3) whether mixing had a lasting effect after animals were resorted into groups of same strain animals. We found that social experience had a profound impact on social behavior. Both Nadia and TM1 individuals engaged in more frequent biting after having been in mixed strain groups compared to pure strain groups. This was true of groups mixed as juveniles, as well as adults, indicating that this response was not dependent on exposure during a critical developmental period. Also, TM1 fish (but not Nadia) having recently been housed in mixed-strain groups were more willing to leave the immediate vicinity of a shoal than were TM1 fish raised in pure strain groups. This change was more pronounced in groups mixed as juveniles than as adults. In addition, the observed changes persisted after mixed groups were separated into pure strain groups for a month. Other behavioral measures including Activity Level, Predator Response and Stress Recovery were unaffected by previous social experience.


Social experience Aggression Boldness Zebrafish 



We thank Erin Churchill for animal husbandry; the animal quarters staff at Indiana University for fish care and maintenance; Padrick Anderson, Awilda Acarón and Jennifer Wright for assistance in scoring videotaped trials; and to Candice Clark, Winnie Ho, Erin Kelso, Saúl Nava, Mayté Ruiz, and Cuauhcihuatl Vital for useful comments and suggestions on earlier versions of this manuscript. This research was supported in part by a National Science Foundation award to EPM (IOB-0543491) and by a National Science Foundation and Idaho University EPSCoR award (EPS-044789) to B. Robison. All experiments comply with current laws of the United States and with the Animal Care Guidelines of Indiana University (BIACUC Protocol Approval #: 05-096).


  1. Adkins-Regan E, Krakauer A (2000) Removal of adult males from the rearing environment increases preference for same-sex partners in the zebra finch. Anim Behav 60:47–53CrossRefGoogle Scholar
  2. Arakawa H (2005) Interaction between isolation rearing and social development on exploratory behavior in male rats. Behav Processes 70:223–234CrossRefGoogle Scholar
  3. Behrmann-Godel J, Gerlach G, Eckmann R (2006) Kin and population recognition in sympatric Lake Constance perch (Perca fluviatilis L.): can assortative shoaling drive population divergence? Behav Ecol Sociobiol 59:461–468CrossRefGoogle Scholar
  4. Black MP, Balthazart J, Baillien M, Grober MS (2005) Socially induced and rapid increases in aggression are inversely related to brain aromatase activity in a sex changing fish, Lythrypnus dalli. Proc Roy Soc London B 272:2435–2440CrossRefGoogle Scholar
  5. Boulcott P, Braithwaite V (2005) Ultraviolet light and visual behaviour in the three-spined stickleback, Gasterosteus aculeatus. Physiol Biochem Zool 78:736–743CrossRefGoogle Scholar
  6. Breder CM, Halpern F (1946) Innate and acquired behavior affecting the aggregation of fishes. Physiol Zool 19:154–192Google Scholar
  7. Brown C, Laland KN (2003) Social learning in fishes: a review. Fish Fisher 4:280–288CrossRefGoogle Scholar
  8. Brown C, Markula A, Laland K (2003) Social learning of prey location in hatchery-reared Atlantic salmon. J Fish Biol 63:738–745CrossRefGoogle Scholar
  9. Brown GE, Brown JA (1993a) Do kin always make better neighbours? The effects of territory quality. Behav Ecol Sociobiol 33:225–231CrossRefGoogle Scholar
  10. Brown GE, Brown JA (1993b) Social dynamics in salmonid fishes: do kin make better neighbours? Anim Behav 45:863–871CrossRefGoogle Scholar
  11. Cremer S, Greenfield MD (1998) Partitioning the components of sexual selection: attractiveness and agonistic behaviour in male wax moths, Achroia grisella. Ethology 104:1–9CrossRefGoogle Scholar
  12. Croft DP, James R, Thomas POR, Hathaway C, Mawdsley D, Laland KN, Krause J (2006) Social structure and co-operative interactions in a wild population of guppies (Poecilia reticulata). Behav Ecol Sociobiol 59:644–650CrossRefGoogle Scholar
  13. Cushing BS, Kramer KM (2005) Mechanisms underlying epigenetic effects of early social experience: the role of neuropeptides and steroids. Neurosci Biobehav Rev 29:1089–1105CrossRefGoogle Scholar
  14. Delaney M, Follet C, Ryan N, Hanney N, Lusk-Yablick J, Gerlach G (2002) Social interaction and distribution of female zebrafish (Danio rerio) in a large aquarium. Biol Bull 203:240–241CrossRefGoogle Scholar
  15. Eaton RC, Farley RD (1974) Spawning cycle and egg production of zebrafish, Brachydanio rerio, in the laboratory. Copeia 1974:195–204CrossRefGoogle Scholar
  16. Engeszer RE, Ryan MJ, Parichy DM (2004) Learned social preferences in zebrafish. Curr Biol 14:881–884CrossRefGoogle Scholar
  17. Franck D, Ribowski A (1987) On the relationship between aggression and social dominance. Ethology 78:223–237Google Scholar
  18. Gerlai R (2003) Zebrafish: an uncharted behavior genetic model. Behav Genet 33:461–468CrossRefGoogle Scholar
  19. Geva S, Hartfelder K, Bloch G (2005) Reproductive division of labor, dominance, and ecdysteroid levels in hemolymph and ovary of the bumble bee Bombus terrestris. J Insect Physiol 51:811–823CrossRefGoogle Scholar
  20. Gibbs PDL, Schmale MC (2000) GFP as a genetic marker scorable throughout the life cycle of transgenic zebrafish. Mar Biotechnol 2:107–125Google Scholar
  21. Griffiths SW (2003) Learned recognition of conspecifics by fishes. Fish Fisher 4:256–268CrossRefGoogle Scholar
  22. Guiasu RC, Dunham DW (1997) Agonistic interactions in male form II Cambarus robustus crayfish and a comparison between male for I and form II intra-form contests. Crustaceana 70:721–736Google Scholar
  23. Hamilton IM, Dill LM (2002) Monopolization of food by zebrafish increases in risky habitats. Can J Zool 80:2164–2169CrossRefGoogle Scholar
  24. Hamilton IM, Dill LM (2003) Group foraging by a kleptoparasitic fish: a strong inference test of social foraging models. Ecology 84:3349–3359CrossRefGoogle Scholar
  25. Harwood AJ, Armstrong JD, Griffiths SW, Metcalfe NB (2002). Sympatric association influences within species dominance relations among juvenile Atlantic salmon and brown trout. Anim Behav 64:85–95CrossRefGoogle Scholar
  26. Hintze J (2001) Number Cruncher Statistical Software (NCSS). Kaysville, UTGoogle Scholar
  27. Hoare DJ, Krause J (2003) Social organization, shoal structure and information transfer. Fish Fisher 4:269–279CrossRefGoogle Scholar
  28. Kodric-Brown A, Johnson SC (2002) Ultraviolet reflectance patterns of male guppies enhance their attractiveness to females. Anim Behav 63:391–396CrossRefGoogle Scholar
  29. Kolm N, Hoffman EA, Olsson J, Berglund A, Jones AG (2005) Group stability and homing behavior but no kin group structures in a coral reef fish. Behav Ecol 16:521–527CrossRefGoogle Scholar
  30. Leimar O, Enquist M (1984) Effects of asymmetries in owner-intruder conflicts. J Theoret Biol 111:475–491CrossRefGoogle Scholar
  31. Margulis SW, Nabong M, Alaks G, Walsh A, Lacy RC (2005) Effects of early experience on subsequent parental behaviour and reproductive success in oldfield mice, Peromyscus polionotus. Anim Behav 69:627–634CrossRefGoogle Scholar
  32. Marks C, West TN, Bagatto B, Moore FBG (2005) Developmental environment alters conditional aggression in zebrafish. Copeia 2005:901–908CrossRefGoogle Scholar
  33. Moretz JA (2003) Aggression and RHP in the northern swordtail fish, Xiphophorus cortezi: the relationship between size and contest dynamics in male–male competition. Ethology 109:995–1008CrossRefGoogle Scholar
  34. Moretz JA, Morris MR (2003) Evolutionarily labile responses to a signal of aggressive intent. Proc Roy Soc London B 270:2271–2277CrossRefGoogle Scholar
  35. Pifferer F, Blázquez M, Navarro L, Gonzalez A (2005) Genetic, endocrine and environmental components of sex determination and differentiation in the European sea bass (Dicentrarchus labrax L.). Gen Comparative Endocrinol 142:102–110CrossRefGoogle Scholar
  36. Pitcher TJ, Green DA, Magurran AE (1986) Dicing with death: predator inspection behavior in minnow shoals. J Fish Biol 28:439–448CrossRefGoogle Scholar
  37. Pritchard VL (2001) Behaviour and morphology of the zebrafish, Danio rerio. PhD dissertation. University of LeedsGoogle Scholar
  38. 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
  39. Robison BD, Rowland W (2005) Zebrafish (Danio rerio) as a model organism in conservation biology: behavioral variation among wild and domesticated strains. Can J Fisher Aqua Sci 62:2046–2054CrossRefGoogle Scholar
  40. Rosenthal GG, Ryan MJ (2005) Assortative preferences for stripes in danios. Anim Behav 70:1063–1066CrossRefGoogle Scholar
  41. Russell ST, Kelley JL, Graves JA, Magurran AE (2004) Kin structure and shoal composition dynamics in the guppy, Poecilia reticulata. Oikos 106:520–526CrossRefGoogle Scholar
  42. Snekser JL, McRobert SP, Murphy CE, Clotfelter ED (2006) Aggregation behavior in wildtype and transgenic zebrafish. Ethology 112:181–187CrossRefGoogle Scholar
  43. Spence R, Smith C (2005) Male territoriality mediates density and sex ratio effects on oviposition in the zebrafish, Danio rerio. Anim Behav 69:1317–1323CrossRefGoogle Scholar
  44. Westerfield M (1995) The zebrafish book. Institute of Neuroscience, University of Oregon, USAGoogle Scholar
  45. Witte DJ, Ryan MJ (2002) Mate choice copying in the sailfin molly, Poecilia latipinna, in the wild. Anim Behav 63:943–949CrossRefGoogle Scholar
  46. Wright D, Rimmer LB, Pritchard VL, Krause J, Butlin R (2003) Inter and intra-population variation in shoaling and boldness in the zebrafish (Danio rerio). Naturwissenschaften 90:374–377CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Jason A. Moretz
    • 1
    Email author
  • Emília P. Martins
    • 1
  • Barrie D. Robison
    • 2
  1. 1.Department of Biology and Center for the Integrative Study of Animal BehaviorIndiana UniversityBloomingtonUSA
  2. 2.Department of Biological Sciences and Center for Reproductive BiologyUniversity of IdahoMoscowUSA

Personalised recommendations