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Behavioral Ecology and Sociobiology

, Volume 68, Issue 4, pp 537–549 | Cite as

Social experience during adolescence influences how male zebra finches (Taeniopygia guttata) group with conspecifics

  • Tim RuplohEmail author
  • Hans-Joachim Bischof
  • Nikolaus von Engelhardt
Original Paper

Abstract

Group-living animals rely on social skills which ensure beneficial interaction and prevent harmful ones with conspecifics. In a previous experiment, we demonstrated that male zebra finches reared in groups during adolescence show consistently less courtship and aggressive behaviour as adults than pair-reared males. Here we tested whether such differences affect how they group with conspecifics, as an indicator of their social integration. Zebra finches were kept in pairs (male–female or male–male) or mixed-sex groups (three males and three females) during adolescence and were introduced to an established group of unknown conspecifics during adulthood. Male courtship and aggressive behaviour were quantified directly after introduction to the group and 48 h later. At the same time, male position in relation to other birds and the number of birds in proximity were recorded. Males that grew up in a small mixed-sex group during adolescence spent more time within groups, were observed in bigger groups and lost less weight than males raised in pairs, indicating that an enriched social environment during early development may facilitate social integration. However, we observed no differences in courtship and aggressive behaviour that could predict the differences in grouping behaviour of pair- and group-reared males. We discuss alternative explanations for the difference in grouping and how to test these in future research.

Keywords

Social competence Social integration Social experience Adolescence Phenotypic plasticity Gregariousness 

Notes

Acknowledgements

We thank Ursula Kodytek, Brigitta Otte, Ursula Rennemann, Kristina Ruhe, Jana Derbogen, Stefanie Taube, Uwe Dettmer, Werner Jamin, Michael Meyerhoff and Sebastian Dietrich for taking care of the animals. We thank Suzanne von Engelhardt for polishing the language of the manuscript. This project was supported by a grant from the German Research Foundation to Hans-Joachim Bischof and Nikolaus von Engelhardt (DFG; FOR 1232: BI 245/20-1).

Ethical standards

According to German animal protection laws, social rearing conditions and behavioural tests applied in this study are not considered experimental procedures that require specific approval by an ethical committee. Animal facilities were approved (dated 18 April 2002) for keeping and breeding zebra finches for research purposes by the local government authority responsible for health, veterinary and food monitoring (Gesundheits-, Veterinär- und Lebensmittelüberwachungsamt Stadt Bielefeld).

Zebra finches are highly social birds that roost and breed together in large colonies. The social group sizes in the present experiment are thus representative of what may occur in a natural situation. Zebra finches are generally tolerant of conspecifics and excessive and severe aggression occurs only rarely, if at all. In the present experiment, only low-intensity aggressive behaviour such as threats and chases were observed, all occurring with modest frequency. The experimental setup ensured enough space to allow birds to easily escape from any antagonistic interaction. An intervention by the experimenter to prevent physical harm to the animals was not necessary at any time. The number and distribution of food and water dispensers assured access to food and water for all birds without risk of competitive exclusion, and all experimental animals were observed to feed during the observation periods. It is thus unlikely that the observed changes in body weight are the result of an inability to reach food or water.

All birds were visually inspected on a daily basis (including weekends) by the experimenter and/or an animal caretaker. Any injuries or other health issues (recognisable by fluffed up or lethargic appearance) would have resulted in immediate removal from the experimental setting, but this was not necessary at any time.

After the experiment, stimulus birds were housed in large aviaries (3 × 3 × 3 m) separated by sex. Experimental males were individually caged and monitored for at least 1 week before being given the opportunity to breed in large outdoor aviaries. During this week, all experimental males reached their pre-experimental weight again.

Further details of breeding and housing conditions are described in the respective method sections.

References

  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 60:47–53PubMedCrossRefGoogle Scholar
  2. Arnold C, Taborsky B (2010) Social experience in early ontogeny has lasting effects on social skills in cooperatively breeding cichlids. Anim Behav 79:621–630CrossRefGoogle Scholar
  3. Banerjee SB, Arterbery AS, Fergus DJ, Adkins-Regan E (2012) Deprivation of maternal care has long-lasting consequences for the hypothalamic-pituitary-adrenal axis of zebra finches. Proc R Soc Lond B 279:759–766CrossRefGoogle Scholar
  4. Benus RF, Henkelmann C (1998) Litter composition influences the development of aggression and behavioural strategy in male Mus domesticus. Behaviour 135:1229–1249CrossRefGoogle Scholar
  5. Bergman TJ, Beehner JC, Cheney DL, Seyfarth RM (2003) Hierarchical classification by rank and kinship in baboons. Science 302:1234–1236PubMedCrossRefGoogle Scholar
  6. Bhatnagar S, Vining C, Iyer V, Kinni V (2006) Changes in hypothalamic-pituitary-adrenal function, body temperature, body weight and food intake with repeated social stress exposure in rats. J Neuroendocrinol 18:13–24PubMedCrossRefGoogle Scholar
  7. Bischof HJ (1994) Sexual imprinting as a two-stage process. In: Hogan JA, Bolhuis JJ (eds) Causal mechanisms of behavioural development. Cambridge University Press, Cambridge, pp 82–87CrossRefGoogle Scholar
  8. Bischof HJ (1997) Song learning, filial imprinting, and sexual imprinting: three variations of a common theme? Res-Tokyo 18:133–146Google Scholar
  9. Blakemore SJ (2008) The social brain in adolescence. Nat Rev Neurosci 9:267–277PubMedCrossRefGoogle Scholar
  10. Buwalda B, Kole MHP, Veenema AH, Huininga M, de Boer SF, Korte SM, Koolhaas JM (2005) Long-term effects of social stress on brain and behavior: a focus on hippocampal functioning. Neurosci Biobehav R 29:83–97CrossRefGoogle Scholar
  11. Buwalda B, Geerdink M, Vidal J, Koolhaas JM (2011) Social behavior and social stress in adolescence: a focus on animal models. Neurosci Biobehav R 35:1713–1721CrossRefGoogle Scholar
  12. Chapman BB, Ward AJW, Krause J (2008) Schooling and learning: early social environment predicts social learning ability in the guppy, Poecilia reticulata. Anim Behav 76:923–929CrossRefGoogle Scholar
  13. Criscuolo F, Monaghan P, Proust A, Skorpilova J, Laurie J, Metcalfe NB (2011) Costs of compensation: effect of early life conditions and reproduction in flight performance in zebra finches. Oecologia 167:315–323PubMedCrossRefGoogle Scholar
  14. Cuthill IC, Hunt S, Cleary C, Clark C (1997) Colour band, dominance, and body mass regulation in male zebra finches (Taeniopygia guttata). Proc R Soc Lond B 264:1093–1099CrossRefGoogle Scholar
  15. Cyr NE, Earle K, Tam C, Romero LM (2007) The effect of chronic psychological stress on corticosterone, plasma metabolites, and immune responsiveness in European starlings. Gen Comp Endocrinol 154:59–66PubMedCrossRefGoogle Scholar
  16. Delville Y, Melloni RH Jr, Ferris CF (1998) Behavioral and neurobiological consequences of social subjugation during puberty in golden hamsters. J Neurosci 18:2667–2672PubMedGoogle Scholar
  17. Ekman JB, Lilliendahl K (1993) Using priority to food access: fattening strategies in dominance-structured willow tit (Parus montanus) flocks. Behav Ecol 4:232–238CrossRefGoogle Scholar
  18. Ferris C, Messenger T, Sullivan R (2005) Behavioral and neuroendocrine consequences of social subjugation across adolescence and adulthood. Front Zool 2:7PubMedCentralPubMedCrossRefGoogle Scholar
  19. Gersick AS, Snyder-Mackler N, White DJ (2012) Ontogeny of social skills-social complexity improves mating and competitive strategies in male cowbirds. Anim Behav 83:1171–1177CrossRefGoogle Scholar
  20. Gil D, Naguib M, Riebel K, Rutstein A, Gahr M (2006) Early condition, song learning, and the volume of song brain nuclei in the zebra finch (Taeniopygia guttata). J Neurobiol 66:1602–1612PubMedCrossRefGoogle Scholar
  21. Gladstone GL, Parker GB, Malhi GS (2006) Do bullied children become anxious and depressed adults? A cross-sectional investigation of the correlates of bullying and anxious depression. J Nerv Ment Dis 194:201–208PubMedCrossRefGoogle Scholar
  22. Godde S, Humbert L, Côté SD, Réale D, Whitehead H (2013) Correcting for the impact of gregariousness in social network analyses. Anim Behav 85:553–558CrossRefGoogle Scholar
  23. Goodson JL, Kingsbury MA (2011) Nonapeptides and the evolution of social group sizes in birds. Front Neuroanat 5:13PubMedCentralPubMedCrossRefGoogle Scholar
  24. Goodson JL, Kelly AM, Kingsbury MA (2012) Evolving nonapeptide mechanisms of gregariousness and social diversity in birds. Horm Behav 61:239–250PubMedCentralPubMedCrossRefGoogle Scholar
  25. Jones AE, ten Cate C, Slater PJB (1996) Early experience and plasticity of song in adult male zebra finches. J Comp Psychol 110:354–369CrossRefGoogle Scholar
  26. Kaiser S, Harderthauer S, Sachser N, Hennessy MB (2007) Social housing conditions around puberty determine later changes in plasma cortisol levels and behavior. Physiol Behav 90:405–411PubMedCrossRefGoogle Scholar
  27. Karino K (1995) Effective timing of male courtship displays for female mate choice in a territorial damselfish Stegastes nigricans. Jpn J Ichthyol 42:173–180Google Scholar
  28. Kelly AM, Kingsbury MA, Hoffbuhr K, Schrock SE, Waxman B, Kabelik D, Thompson RR (2011) Vasotocin neurons and septal V1a-like receptors potently modulate songbird flocking and responses to novelty. Horm Behav 60:12–21PubMedCentralPubMedCrossRefGoogle Scholar
  29. Koolhaas JM, Bartollimucci A, Buwalda B, de Boer SF, Flügge G, Korte SM, Meerlo P, Murison R, Olivier B, Palanza P, Richter-Levin G, Sgoifo A, Steimer T, Stiedl O, van Dijk G, Wöhr M, Fuchs E (2011) Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav R 35:1291–1301CrossRefGoogle Scholar
  30. Krause ET, Honarmand M, Wetzel J, Naguib M (2009) Early fasting is long lasting: differences in early nutritional conditions reappear under stressful conditions in adult female zebra finches. PloS ONE 4:e5015PubMedCentralPubMedCrossRefGoogle Scholar
  31. Lauay C, Gerlach NM, Adkins-Regan E, Devoogd TJ (2004) Female zebra finches require early song exposure to prefer high-quality song as adults. Anim Behav 68:1249–1255CrossRefGoogle Scholar
  32. Lürzel S, Kaiser S, Sachser N (2010) Social interaction, testosterone, and stress responsiveness during adolescence. Physiol Behav 99:40–46PubMedCrossRefGoogle Scholar
  33. Lürzel S, Kaiser S, Sachser N (2011) Social interaction decreases stress responsiveness during adolescence. Psychoneuroendocrinology 36:1370–1377PubMedCrossRefGoogle Scholar
  34. Mariette MM, Griffith SC (2012) Conspecific attraction and nest site selection in a nomadic species, the zebra finch. Oikos 121:823–834CrossRefGoogle Scholar
  35. Mariette MM, Griffith SC (2013) Does coloniality improve foraging efficiency and nestling provisioning? A field experiment in the wild Zebra Finch. Ecology 94:325–335PubMedCrossRefGoogle Scholar
  36. Martin P, Bateson P (1993) Measuring behaviour: an introductory guide, 2nd edn. Cambridge University Press, Cambridge, UKCrossRefGoogle Scholar
  37. McCormick CM, Smith C, Mathews IZ (2008) Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behav Brain Res 187:228–238PubMedCrossRefGoogle Scholar
  38. McNamara JM, Houston AI (1990) The value of fat reserves and the tradeoff between starvation and predation. Acta Biotheor 38:37–61PubMedCrossRefGoogle Scholar
  39. Meerlo P, Overkamp GJF, Daan S, van den Hoofdakker RH, Koolhaas JM (1996) Changes in behaviour and body weight following a single or double social defeat in rats. Stress 1:21–32PubMedCrossRefGoogle Scholar
  40. Naguib M, Flörcke C, van Oers K (2011) Effects of social conditions during early development on stress response and personality traits in great tits (Parus major). Dev Psychobiol 53:592–600PubMedCrossRefGoogle Scholar
  41. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956PubMedGoogle Scholar
  42. Nelson EE, Leibenluft E, McClure EB, Pine DS (2005) The social re-orientation of adolescence: a neuroscience perspective on the process and its relation to psychopathology. Psychol Med 35:163–174PubMedCrossRefGoogle Scholar
  43. Oliveira RF (2009) Social behavior in context: hormonal modulation of behavioral plasticity and social competence. Integr Comp Biol 49:423–440PubMedCrossRefGoogle Scholar
  44. Pröve E (1987) Verhalten und Hormone: funktionelle Aspekte der Wechselbeziehungen von Hormonen und Verhaltensweisen. Verh Dtsch Zool Ges 80:33–44Google Scholar
  45. Rich EL, Romero LM (2005) Exposure to chronic stress downregulates corticosterone responses to acute stressors. Am J Physiol-Reg I 288:1628–1636Google Scholar
  46. Riebel K, Spierings MJ, Holveck MJ, Verhulst S (2012) Phenotypic plasticity of avian social-learning strategies. Anim Behav 84:1533–1539CrossRefGoogle Scholar
  47. Rose-Krasnor L (1997) The nature of social competence: a theoretical review. Soc Dev 6:111–135CrossRefGoogle Scholar
  48. Ruploh T, Bischof HJ, von Engelhardt N (2013) Adolescent social environment shapes sexual and aggressive behaviour of adult male zebra finches (Taeniopygia guttata). Behav Ecol Sociobiol 67:175–184CrossRefGoogle Scholar
  49. Sachser N (1993) The ability to arrange with conspecifics depends on social experiences around puberty. Physiol Behav 53:539–544PubMedCrossRefGoogle Scholar
  50. Sachser N, Lick C (1989) Social stress in guinea pigs. Physiol Behav 46:137–144PubMedCrossRefGoogle Scholar
  51. Sachser N, Lick C (1991) Social experience, behavior, and stress in guinea pigs. Physiol Behav 50:83–90PubMedCrossRefGoogle Scholar
  52. Sachser N, Pröve E (1988) Plasma-testosterone development in colony and individually housed male guinea pigs. Ethology 79:62–70CrossRefGoogle Scholar
  53. Sachser N, Renninger SV (1993) Coping with new social situations: the role of social rearing in guinea pigs. Ethol Ecol Evol 5:65–74CrossRefGoogle Scholar
  54. Sachser N, Hennessy MB, Kaiser S (2011) Adaptive modulation of behavioural profiles by social stress during early phases of life and adolescence. Neurosc Biobehav R 35:1518–1533CrossRefGoogle Scholar
  55. Sachser N, Kaiser S, Hennessy MB (2013) Behavioural profiles are shaped by social experience: when, how and why. Philos Trans R Soc B 368:20120344CrossRefGoogle Scholar
  56. Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89PubMedGoogle Scholar
  57. Silcox AP, Evans SM (1982) Factors affecting the formation and maintenance of pair bonds in the zebra finch, Taeniopygia guttata. Anim Behav 30:1237–1243CrossRefGoogle Scholar
  58. Sossinka R, Böhner J (1980) Song types in the zebra finch Poephilia guttata castanotis. Z Tierphysiol 53:123–132Google Scholar
  59. Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav R 24:417–463CrossRefGoogle Scholar
  60. Sterlemann V, Rammes G, Wolf M, Liebl C, Ganea K, Müller MB, Schmidt MV (2010) Chronic social stress during adolescence induces cognitive impairment in aged mice. Hippocampus 20:540–549PubMedGoogle Scholar
  61. Susman EJ (1997) Modeling developmental complexity in adolescence, hormones and behaviour in context. J Res Adolesc 7:283–306CrossRefGoogle Scholar
  62. Taborsky B, Oliveira RF (2012) Social competence: an evolutionary approach. Trends Ecol Evol 27:679–688PubMedCrossRefGoogle Scholar
  63. Taborsky B, Arnold A, Junker J, Tschopp A (2012) The early social environment affects social competence in a cooperative breeder. Anim Behav 83:1067–1074PubMedCentralPubMedCrossRefGoogle Scholar
  64. Tchernichovski O, Nottenbohm F (1998) Social inhibition of song imitation among sibling male zebra finches. Proc Natl Acad Sci U S A 95:8951–8956PubMedCentralPubMedCrossRefGoogle Scholar
  65. White DJ, Gros-Louis J, King AP, Papakhian MA, West MJ (2007) Constructing culture in cowbirds (Molothrus ater). J Comp Psychol 121:113–122PubMedCrossRefGoogle Scholar
  66. White DJ, Gersick AS, Freed-Brown G, Snyder-Mackler N (2010) The ontogeny of social skills: experimental increases in social complexity enhance reproductive success in adult cowbirds. Anim Behav 79:385–390CrossRefGoogle Scholar
  67. Witter MS, Swaddle JP (1995) Dominance, competition, and energetic reserves in European starling, Sturnus vulgaris. Behav Ecol 6:343–348CrossRefGoogle Scholar
  68. Young LJ (2002) The neurobiology of social recognition, approach and avoidance. Biol Psychiatry 51:18–26PubMedCrossRefGoogle Scholar
  69. Zann RA (1996) The zebra finch: a synthesis of field and laboratory studies, 1st edn. Oxford University Press, OxfordGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Tim Ruploh
    • 1
    Email author
  • Hans-Joachim Bischof
    • 1
  • Nikolaus von Engelhardt
    • 1
  1. 1.Lehrstuhl VerhaltensforschungUniversität BielefeldBielefeldGermany

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