Behavioral Ecology and Sociobiology

, Volume 68, Issue 5, pp 871–878 | Cite as

Mirror, mirror on the wall: the predictive value of mirror tests for measuring aggression in fish

  • Valentina Balzarini
  • Michael Taborsky
  • Sandro Wanner
  • Felizia Koch
  • Joachim G. Frommen
Methods

Abstract

The behaviour of animals towards their mirror image (“mirror test”) is routinely used as a proxy to measure aggression levels, especially in fish. The lack of evidence for visual self-recognition in fish supports this method. However, recent work points towards different hormonal and gene expression responses when fish are exposed either to conspecific opponents or to their mirror image, urging for validation of this widespread method. Here, we test the predictive value of mirror tests in three sympatric cichlid species from Lake Tanganyika: the cooperative breeder Neolamprologus pulcher, the polygamous shell brooder Telmatochromis vittatus and the monogamous, biparental piscivore Lepidiolamprologus elongatus. In particular, we compare differences in restrained and overt aggression levels for individuals of each species when confronted with a mirror or a live conspecific. The three species differed in response to the two contest situations. While in N. pulcher both aggressive responses were correlated between the mirror test and the live opponent fight, there was no such relationship in T. vittatus and L. elongatus. Thus, the mirror test appears to be a suitable surrogate for intraspecific aggression in N. pulcher, while aggression against a mirror image has limited predictive value for intraspecific aggression in the other two species. These results underline the importance of validating the mirror test’s predictive value in a study species before drawing conclusions from mirror tests about aggressiveness under natural, social conditions.

Keywords

Neolamprologus pulcher Cichlid fish Animal personality Behavioural syndrome Copying style 

References

  1. Andrews E (1996) Slate-colored junco response to mirror. Bird-Banding 37:206CrossRefGoogle Scholar
  2. Arnott G, Elwood RW (2008) Information gathering and decision making about resource value in animal contests. Anim Behav 76:529–542CrossRefGoogle Scholar
  3. Arnott G, Elwood R (2009) Probing aggressive motivation in a cichlid fish. Biol Lett 5:762–764PubMedCentralPubMedCrossRefGoogle Scholar
  4. Arnott G, Ashton C, Elwood RW (2011) Lateralization of lateral displays in convict cichlids. Biol Lett 7:683–685PubMedCentralPubMedCrossRefGoogle Scholar
  5. Bakker TCM, Sevenster P (1983) Determinants of dominance in male sticklebacks (Gasterosteus aculeatus L.). Behaviour 86:55–71CrossRefGoogle Scholar
  6. Balshine S, Leach B, Neat F, Reid H, Taborsky M, Werner N (2001) Correlates of group size in a cooperatively breeding cichlid fish (Neolamprologus pulcher). Behav Ecol Sociobiol 50:134–140CrossRefGoogle Scholar
  7. Boon AK, Reale D, Boutin S (2008) Personality, habitat use, and their consequences for survival in North American red squirrels Tamiasciurus hudsonicus. Oikos 117:1321–1328CrossRefGoogle Scholar
  8. Brawn VM (1961) Aggressive behaviour in the cod (Gadus calalris L.). Behaviour 18:107–147CrossRefGoogle Scholar
  9. Bruintjes R, Taborsky M (2008) Helpers in a cooperative breeder pay a high price to stay: effects of demand, helper size and sex. Anim Behav 75:1843–1850CrossRefGoogle Scholar
  10. Chervet N, Zöttl M, Schürch R, Taborsky M, Heg D (2011) Repeatability and heritability of behavioural types in a social cichlid. Int J Evol Biol 2011:321729PubMedCentralPubMedCrossRefGoogle Scholar
  11. Constanz GD (1975) Behavioural ecology of mating in the male Gila topminnow, Poecilipsis occidentalis (Cyprinodontiformes: Poeciliidae). Ecology 56:966–973CrossRefGoogle Scholar
  12. Craft BB, Velkey AJ, Szalda-Petree A (2003) Instrumental conditioning of choice behavior in male Siamese fighting fish (Betta splendens). Behav Process 63:171–175CrossRefGoogle Scholar
  13. de Veer MW, van den Bos R (1999) A critical review of methodology and interpretation of mirror self-recognition research in nonhuman primates. Anim Behav 58:459–468PubMedCrossRefGoogle Scholar
  14. Desjardins JK, Fernald RD (2010) What do fish make of mirror images? Biol Lett 6:744–747PubMedCentralPubMedCrossRefGoogle 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 76:1128–1138PubMedCrossRefGoogle Scholar
  16. Dingemanse NJ, Dochtermann NA, Nakagawa S (2012) Defining behavioural syndromes and the role of “syndrome deviation” in understanding their evolution. Behav Ecol Sociobiol 66:1543–1548CrossRefGoogle Scholar
  17. Drodz JK, Viscek J, Brudzynski SM, Mercier JA (2006) Behavioral responses of crayfish to a reflective environment. J Crustac Biol 26:463–473CrossRefGoogle Scholar
  18. Duftner N, Sefc KM, Koblmüller S, Salzburger W, Taborsky M, Sturmbauer C (2007) Parallel evolution of facial stripe patterns in the Neolamprologus brichardi/pulcher species complex endemic to Lake Tanganyika. Mol Phylogenet Evol 45:706–715PubMedCrossRefGoogle Scholar
  19. Earley RL, Hsu Y, Wolf LL (2000) The use of standard aggression testing methods to predict combat behaviour and contest outcome in Rivulus marmoratus dyads (Teleostei: Cyprinodontidae). Ethology 106:743–761CrossRefGoogle Scholar
  20. Frostman P, Sherman PT (2004) Behavioral response to familiar and unfamiliar neighbors in a territorial cichlid, Neolamprologus pulcher. Ichthyol Res 51:283–285CrossRefGoogle Scholar
  21. Fryer G, Iles TD (1972) Cichlid fishes of the great lakes of Africa: their biology and evolution. Oliver and Boyd, EdinburghGoogle Scholar
  22. Gallup GG (1968) Mirror-image stimulation. Psychol Bull 70:782–793PubMedCrossRefGoogle Scholar
  23. Gashagaza M (1991) Diversity of breeding habits in lamprologini cichlids in Lake Tanganyika. Physiol Ecol Japan 28:29–65Google Scholar
  24. Gherardi F (2006) Fighting behavior in hermit crabs: the combined effect of resource-holding potential and resource value in Pagurus longicarpus. Behav Ecol Sociobiol 59:500–510CrossRefGoogle Scholar
  25. Grantner A, Taborsky M (1998) The metabolic rates associated with resting, and with the performance of agonistic, submissive and digging behaviours in the cichlid fish Neolamprologus pulcher (Pisces: Cichlidae). J Comp Physiol 168:427–433CrossRefGoogle Scholar
  26. Hamilton IM, Heg D, Bender N (2005) Size differences within a dominance hierarchy influence conflict and help in a cooperatively breeding cichlid. Behaviour 142:1591–1613CrossRefGoogle Scholar
  27. Heg D, Brouwer L, Bachar Z, Taborsky M (2005) Large group size yields group stability in the cooperatively breeding cichlid Neolamprologus pulcher. Behaviour 142:1615–1641CrossRefGoogle Scholar
  28. Heg D, Heg-Bachar Z, Brouwer L, Taborsky M (2008) Experimentally induced helper dispersal in colonially breeding cooperative cichlids. Environ Biol Fish 83:191–206CrossRefGoogle Scholar
  29. Heg D, Schürch R, Rothenberger S (2011) Behavioral type and growth rate in a cichlid fish. Behav Ecol 22:1227–1233CrossRefGoogle Scholar
  30. Hirschenhauser K, Wittek M, Johnston P, Möstl E (2008) Social context rather than behavioral output or winning modulates post-conflict testosterone responses in Japanese quail (Coturnix japonica). Physiol Behav 95:457–463PubMedCrossRefGoogle Scholar
  31. Hori M, Yamaoka K, Tamakura K (1983) Abundance and micro-distribution of cichlid fishes on a rocky shore of Lake Tanganyika. Afr Study Monogr 3:25–38Google Scholar
  32. Huntingford FA (1980) A review of the methods used to describe and measure aggressive behaviour in physiological studies. Aggress Behav 6:205–215CrossRefGoogle Scholar
  33. Keenleyside MHA, Yamamoto FT (1962) Territorial behaviour of juvenile Atlantic salmon (Salmo salar L.). Behaviour 19:139–169CrossRefGoogle Scholar
  34. Konings A (1998) Tanganyika cichlids in their natural habitat. Cichlid Press, El Paso, USAGoogle Scholar
  35. Kusayama T, Bischof H, Watanabe S (2000) Responses to mirror-image stimulation in jungle crows (Corvus macrorhynchos). Anim Cogn 3:61–64CrossRefGoogle Scholar
  36. Lissmann H (1932) Die Umwelt des Kampffisches (Betta splendens Regan). Z Vergl Physiol 18:65–111Google Scholar
  37. Matessi G, Matos RJ, Peake TM, Mcgregor PK, Dabelsteen T (2010) Effects of social environment and personality on communication in male Siamese fighting fish in an artificial network. Anim Behav 79:43–49CrossRefGoogle Scholar
  38. May HY, Mercier JA (2007) Duration of socialization influences responses to a mirror: responses of dominant and subordinate crayfish diverge with time of pairing. J Exp Biol 210:4428–4436PubMedCrossRefGoogle Scholar
  39. Mehlis M, Bakker TCM, Langen K, Frommen JG (2009) Cain and Abel reloaded? Kin recognition and male-male aggression in three-spined sticklebacks Gasterosteus aculeatus L. J Fish Biol 75:2154–2162PubMedCrossRefGoogle Scholar
  40. Mitchell JS, Jutzeler E, Heg D, Taborsky M (2009) Dominant members of cooperatively-breeding groups adjust their behaviour in response to the sexes of their subordinates. Behaviour 146:1665–1686CrossRefGoogle Scholar
  41. Ochi H, Yanagisawa Y (1998) Commensalism between cichlid fishes through differential tolerance of guarding parents towards intruders. J Fish Biol 52:985–996CrossRefGoogle Scholar
  42. Ota K, Kohda M (2005) Description of alternative male reproductive tactics in a shell-brooding cichlid, Telmatochromis vittatus, in Lake Tanganyika. J Ethol 24:9–15CrossRefGoogle Scholar
  43. Pepperberg IM, Garcia SE, Jackson EC, Marconi S (1995) Mirror use by African grey parrots (Psittacus erithacus). J Comp Psychol 109:182–195CrossRefGoogle Scholar
  44. Plotnik JM, de Waal FBM, Moore D, Reiss D (2010) Self-recognition in the Asian elephant and future directions for cognitive research with elephants in zoological settings. Zoo Biol 29:179–191PubMedCrossRefGoogle Scholar
  45. Prior H, Schwarz A, Gu O, Güntürkün O (2008) Mirror-induced behavior in the magpie (Pica pica): evidence of self-recognition. PLoS Biol 6:e202PubMedCentralPubMedCrossRefGoogle Scholar
  46. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing 1:409, http://cran.r-project.org/
  47. Reddon AR, O’Connor CM, Marsh-Rollo SE, Balshine S (2012) Effects of isotocin on social responses in a cooperatively breeding fish. Anim Behav 84:753–760CrossRefGoogle Scholar
  48. Riebli T, Avgan B, Bottini A, Duc C, Taborsky M, Heg D (2011) Behavioural type affects dominance and growth in staged encounters of cooperatively breeding cichlids. Anim Behav 81:313–323CrossRefGoogle Scholar
  49. Riebli T, Taborsky M, Chervet N, Apolloni N, Zürcher Y, Heg D (2012) Behavioural type, status and social context affect behaviour and resource allocation in cooperatively breeding cichlids. Anim Behav 84:925–936CrossRefGoogle Scholar
  50. Schilhab TSS (2004) What mirror self-recognition in nonhumans can tell us about aspects of self. Biol Philos 19:111–126CrossRefGoogle Scholar
  51. Schürch R, Heg D (2010) Life history and behavioral type in the highly social cichlid Neolamprologus pulcher. Behav Ecol 21:588–598CrossRefGoogle Scholar
  52. Stockermans BC, Hardy ICW (2013) Subjective and objective components of resource value additively increase aggression in parasitoid contests. Biol Lett 9:20130391PubMedCentralPubMedCrossRefGoogle Scholar
  53. Sturmbauer C, Verheyen E, Meyer A (1994) Mitochondrial phylogeny of the Lamprologini, the major substrate spawning lineage of cichild fishes from Lake Tanganyika in eastern Africa. Mol Biol Evol 11:691–703PubMedGoogle Scholar
  54. Taborsky M (1984) Broodcare helpers in the cichlid fish Lamprologus brichardi: their costs and benefits. Anim Behav 32:1236–1252CrossRefGoogle Scholar
  55. Taborsky M (1985) Breeder-helper conflict in a cichlid fish with broodcare helpers: an experimental analysis. Behaviour 95:45–75CrossRefGoogle Scholar
  56. Taborsky M, Grantner A (1998) Behavioural time-energy budgets of cooperatively breeding Neolamprologus pulcher (Pisces: Cichlidae). Anim Behav 56:1375–1382PubMedCrossRefGoogle Scholar
  57. Taborsky M, Limberger D (1981) Helpers in fish. Behav Ecol Sociobiol 8:143–145CrossRefGoogle Scholar
  58. Taves MD, Desjardins JK, Mishra S, Balshine S (2009) Androgens and dominance: sex-specific patterns in a highly social fish (Neolamprologus pulcher). Gen Comp Endocrinol 161:202–207PubMedCrossRefGoogle Scholar
  59. Tinbergen N (1951) The study of instinct. Clarendon/Oxford University Press, New YorkGoogle Scholar
  60. Van Dyk DA, Evans CS (2008) Opponent assessment in lizards: examining the effect of aggressive and submissive signals. Behav Ecol 19:895–901CrossRefGoogle Scholar
  61. Verbeek P, Iwamoto T, Murakami N (2007) Differences in aggression between wild-type and domesticated fighting fish are context dependent. Anim Behav 73:75–83CrossRefGoogle Scholar
  62. Vøllestad LA, Quinn TP (2003) Trade-off between growth rate and aggression in juvenile coho salmon, Oncorhynchus kisutch. Anim Behav 66:561–568CrossRefGoogle Scholar
  63. Waal FBM D, Dindo M, Freeman CA, Hall MJ (2005) The monkey in the mirror: hardly a stranger. Proc Natl Acad Sci U S A 102:11140–11147CrossRefGoogle Scholar
  64. Wilson AJ, de Boer M, Arnott G, Grimmer A (2011) Integrating personality research and animal contest theory: aggressiveness in the green swordtail Xiphophorus helleri. PLoS ONE 6:e28024PubMedCentralPubMedCrossRefGoogle Scholar
  65. Witsenburg F, Schürch R, Otti O, Heg D (2010) Behavioural types and ecological effects in a natural population of the cooperative cichlid Neolamprologus pulcher. Anim Behav 80:757–767CrossRefGoogle Scholar
  66. Zajonc R (1966) Social psychology: an experimental approach. BelmontGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Valentina Balzarini
    • 1
  • Michael Taborsky
    • 1
  • Sandro Wanner
    • 1
  • Felizia Koch
    • 1
  • Joachim G. Frommen
    • 1
  1. 1.Department of Behavioural Ecology, Institute of Ecology and EvolutionUniversity of BernHinterkappelenSwitzerland

Personalised recommendations