Repeatability of lateralisation in mosquitofish Gambusia holbrooki despite evidence for turn alternation in detour tests

Abstract

Akin to handedness in humans, some animals show a preference for moving to the left or right. This is often attributed to lateralised cognitive functions and eye dominance, which, in turn, influences their behaviour. In fishes, behavioural lateralisation has been tested using detour mazes for over 20 years. Studies report that certain individuals are more likely to approach predators or potential mates from one direction. These findings imply that the lateralisation behaviour of individuals is repeatable, but this is rarely confirmed through multiple testing of each individual over time. Here we quantify the repeatability of turning behaviour by female mosquitofish (Gambusia holbrooki) in a double sided T-maze. Each female was tested three times in each of six treatments: when approaching other females, males, or an empty space; and when able to swim freely or when forced to choose by being herded from behind with a net. Although there was no turning bias based on the mean population response, we detected significant repeatability of lateralisation in five of the six treatments (R = 0.251–0.625). This is noteworthy as we also found that individuals tended to alternate between left and right turns, meaning that they tend to move back and forth along one wall of the double-sided T-maze. Furthermore, we found evidence for this wall following when re-analysing data from a previous study. We discuss potential explanations for this phenomenon, and its implications for study design.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Data availability

The datasets and R code generated during the current study are available in supplementary materials. Video footage of the experimental procedure is available from the corresponding author on reasonable request.

References

  1. Agrillo C, Dadda M, Bisazza A (2006) Sexual harassment influences group choice in female mosquitofish. Ethology 112:592–598

    Article  Google Scholar 

  2. Aronson LR, Clark E (1952) Evidences of ambidexterity and laterality in the sexual behaviour of certain Poeciliid fishes. Am Nat 86:161–171

    Article  Google Scholar 

  3. Basil J, Sandeman D (2000) Crayfish (Cherax destructor) use tactile cues to detect and learn topographical changes in their environment. Ethology 106:247–259. https://doi.org/10.1046/j.14390310.2000.00524.x

    Article  Google Scholar 

  4. Bibost AL, Brown C (2013) Laterality influences schooling position in rainbowfish Melanotaenia spp. PLoS ONE 8:80907–80907

    Article  CAS  Google Scholar 

  5. Bibost AL, Brown C (2014) Laterality influences cognitive performance in rainbowfish Melanotaenia duboulayi. Anim Cogn 17:1045–1051

    PubMed  Article  Google Scholar 

  6. Bisazza A, De Santi A (2003) Lateralization of aggression in fish. Behav Brain Res 141:131–136

    PubMed  Article  Google Scholar 

  7. Bisazza A, Vallortigara G (1997) Rotational swimming preferences in mosquitofish: evidence for brain lateralization? Physiol Behav 62:1405–1407

    CAS  PubMed  Article  Google Scholar 

  8. Bisazza A, Pignatti R, Vallortigara G (1997a) Detour tests reveal task- and stimulus-specific behavioural lateralization in mosquitofish (Gambusia holbrooki). Behav Brain Res 89:237–242

    CAS  PubMed  Article  Google Scholar 

  9. Bisazza A, Pignatti R, Vallortigara G (1997b) Laterality in detour behaviour: interspecific variation in poeciliid fish. Anim Behav 54:1273–1281

    CAS  PubMed  Article  Google Scholar 

  10. Bisazza A, Facchin L, Pignatti R, Vallortigara G (1998) Lateralization of detour behaviour in poeciliid fish: the effect of species, gender and sexual motivation. Behav Brain Res 91:157–164

    CAS  PubMed  Article  Google Scholar 

  11. Bisazza A, Cantalupo C, Capocchiano M, Vallortigara G (2000a) Population lateralisation and social behaviour: a study with 16 species of fish. Laterality 5:269–284

    CAS  PubMed  Article  Google Scholar 

  12. Bisazza A, Facchin L, Vallortigara G (2000b) Heritability of lateralization in fish: concordance of right–left asymmetry between parents and offspring. Neuropsychologia 38:907–912

    CAS  PubMed  Article  Google Scholar 

  13. Blois-Heulin C, Crevel M, Boye M, Lemasson A (2012) Visual laterality in dolphins: importance of the familiarity of stimuli. BMC Neurosci 13:9

    PubMed  PubMed Central  Article  Google Scholar 

  14. Brown C (2005) Cerebral lateralisation, “social constraints”, and coordinated anti-predator responses. Behav Brain Sci 28:591–592

    Article  Google Scholar 

  15. Brown C, Gardner C, Braithwaite VA (2004) Population variation in lateralized eye use in the poeciliid Brachyraphis episcopi. Proc R Soc B 271:455–457

    Google Scholar 

  16. Brown C, Western J, Braithwaite VA (2007) The influence of early experience on, and inheritance of, cerebral lateralization. Anim Behav 74:231–238

    Article  Google Scholar 

  17. Byrnes EE, Vila Pouca C, Brown C (2016) Laterality strength is linked to stress reactivity in Port Jackson sharks (Heterodontus portusjacksoni). Behav Brain Res 305:239–246

    PubMed  Article  Google Scholar 

  18. Cantalupo C, Bisazza A, Vallortigara G (1995) Lateralization of predator-evasion response in a teleost fish (Girardinus falcatus). Neuropsychologia 33:1637–1646

    CAS  PubMed  Article  Google Scholar 

  19. Chivers DP, Mccormick MI, Allan BJM, Mitchell MD, Gonçalves EJ, Bryshun R, Ferrari MCO (2016) At odds with the group: changes in lateralization and escape performance reveal conformity and conflict in fish schools. Proc R Soc B 283:20161127

    PubMed  Article  Google Scholar 

  20. Chivers DP, Mccormick MI, Warren DT, Allan BJM, Ramasamy RA, Arvizu BK, Glue M, Ferrari MCO (2017) Competitive superiority versus predation savvy: the two sides of behavioural lateralization. Anim Behav 130:9–15

    Article  Google Scholar 

  21. Creed RP, Miller JR (1990) Interpreting animal wall-following behavior. Experientia 46(7):758–761. https://doi.org/10.1007/BF01939959

    Article  Google Scholar 

  22. Csermely D, Bonati B, Romani R (2010) Lateralisation in a detour test in the common wall lizard (Podarcis muralis). Laterality 15:535–547

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  23. Dadda M, Bisazza A (2006) Does brain asymmetry allow efficient performance of simultaneous tasks? Anim Behav 72:523–529

    Article  Google Scholar 

  24. Dadda M, Bisazza A (2012) Prenatal light exposure affects development of behavioural lateralization in a livebearing fish. Behav Process 91:115–118

    Article  Google Scholar 

  25. Dadda M, Zandonà E, Agrillo C, Bisazza A (2009) The costs of hemispheric specialization in a fish. Proc R Soc B 276:4399–4407

    PubMed  Article  PubMed Central  Google Scholar 

  26. Dale Broder E, Angeloni LM (2014) Predator-induced phenotypic plasticity of laterality. Anim Behav 98:125–130

    Article  Google Scholar 

  27. Davis TR, Smith SDA (2017) Proximity effects of natural and artificial reef walls on fish assemblages. Reg Stud Mar Sci 9:17–23

    Article  Google Scholar 

  28. Dill L (1977) ‘Handedness’ in the Pacific tree frog (Hyla regilla). Can J Zool 55:1926–1929

    Article  Google Scholar 

  29. Domenici P, Allan B, Mccormick MI, Munday PL (2012) Elevated carbon dioxide affects behavioural lateralization in a coral reef fish. Biol Lett 8:78–81

    CAS  PubMed  Article  Google Scholar 

  30. Ferrari MCO, Mccormick MI, Mitchell MD, Allan BJM, Gonçalves EJ, Chivers DP (2017) Daily variation in behavioural lateralization is linked to predation stress in a coral reef fish. Anim Behav 133:189–193

    Article  Google Scholar 

  31. Frasnelli E, Vallortigara G, Rogers LJ (2012) Left-right asymmetries of behaviour and nervous system in invertebrates. Neurosci Biobehav Rev 36(4):1273–1291

    PubMed  Article  Google Scholar 

  32. Fuss T, Nöbel S, Witte K (2019) It’s in the eye of the beholder: visual lateralisation in response to the social environment in poeciliids. J Fish Biol 94:759–771

    PubMed  Article  Google Scholar 

  33. Gatto E, Agrillo C, Brown C, Dadda M (2019) Individual differences in numerical skills are influenced by brain lateralization in guppies (Poecilia reticulata). Intelligence 74:12–17

    Article  Google Scholar 

  34. Giljov A, Karenina K, Malashichev Y (2013) Forelimb preferences in quadrupedal marsupials and their implications for laterality evolution in mammals. BMC Evol Biol 13:61

    PubMed  PubMed Central  Article  Google Scholar 

  35. Hansen M, Schaerf T, Ward A (2015) The effect of hunger on the exploratory behaviour of shoals of mosquitofish Gambusia holbrooki. Behaviour 152:1659–1677

    Article  Google Scholar 

  36. Hänzi S, Straka H (2018) Wall following in Xenopus laevis is barrier-driven. J Comp Physiol A 204(2):183–195. https://doi.org/10.1007/s00359-017-1227-z

    CAS  Article  Google Scholar 

  37. Irving E, Brown C (2013) Examining the link between personality and laterality in a feral guppy Poecilia reticulata population. J Fish Biol 83:311–325

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  38. Juszczak GR, Miller M (2016) Detour behaviour of mice trained with transparent, semitransparent and opaque barriers. PLoS ONE 11:0162018

    Article  CAS  Google Scholar 

  39. Kabadayi C, Bobrowicz K, Osvath M (2017) The detour paradigm in animal cognition. Anim Cogn. https://doi.org/10.1007/s10071-017-1152-0

    Article  PubMed  PubMed Central  Google Scholar 

  40. Kistler C, Hegglin D, Würbel H, König B (2011) Preference for structured environment in zebrafish (Danio rerio) and checker barbs (Puntius oligolepis). Appl Anim Behav Sci 135:318327

    Article  Google Scholar 

  41. Koboroff A, Kaplan G, Rogers LJ (2008) Hemispheric specialization in Australian magpies (Gymnorhina tibicen) shown as eye preferences during response to a predator. Brain Res Bull 76:304–306

    PubMed  Article  Google Scholar 

  42. Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MAW, Blokhuis HJ (1999) Coping styles in animals: current status in behaviour and stressphysiology. Neurosci Biobehav Rev 23:925–935

    CAS  PubMed  Article  Google Scholar 

  43. Loffing F, Hagemann N, Strauss B (2012) Left-handedness in professional and amateur tennis. PLoS ONE 7:49325–49325

    Article  CAS  Google Scholar 

  44. Lopes AF, Morais P, Pimentel M, Rosa R, Munday PL, Gonçalves EJ, Faria AM (2016) Behavioural lateralization and shoaling cohesion of fish larvae altered under ocean acidification. Mar Biol 163:243

    Article  CAS  Google Scholar 

  45. Lucon-Xiccato T, Bisazza A (2017) Individual differences in cognition among teleost fishes. Behav Process 141:184–195

    Article  Google Scholar 

  46. Lucon-Xiccato T, Chivers D, Mitchell M, Ferrari M (2017) Prenatal exposure to predation affects predator recognition learning via lateralization plasticity. Behav Ecol 28:155

    Article  Google Scholar 

  47. MacNeilage PF, Studdert-Kennedy MG, Lindblom B (1987) Primate handedness reconsidered. Behav Brain Sci 10:247–303

    Article  Google Scholar 

  48. Magat M, Brown C (2009) Laterality enhances cognition in Australian parrots. Proc R Soc B 276:4155–4162

    PubMed  Article  Google Scholar 

  49. Malagoli Lanzoni I, Di Michele R, Bartolomei S, Semprini G (2019) Do left-handed players have a strategic advantage in table tennis? Int J Racket Sports Sci 1:61–69

    Google Scholar 

  50. Maulvault AL, Santos L, Paula JR, Camacho C, Pissarra V, Fogaca F, Barbosa V, Alves R, Ferreira PP, Barcelo D, Rodriguez-Mozaz S, Marques A, Diniz M, Rosa R (2018) Differential behavioural responses to venlafaxine exposure route, warming and acidification in juvenile fish (Argyrosomus regius). Sci Total Environ 634:1136–1147

    CAS  PubMed  Article  Google Scholar 

  51. Maximino C, Marques De Brito T, Dias CAGDM, Gouveia A, Morato S (2010) Scototaxis as anxiety-like behaviour in fish. Nat Protoc 5:209–216

    CAS  PubMed  Article  Google Scholar 

  52. McLean S, Morrell LJ (2020) Consistency in the strength of laterality in male, but not female, guppies across different behavioural contexts. Biol Lett 16:20190870

    PubMed  Article  Google Scholar 

  53. Munteanu AM, Starnberger I, Pašukonis A, Bugnyar T, Hödl W, Fitch WT (2016) Take the long way home: Behaviour of a neotropical frog, Allobates femoralis, in a detour task. Behav Process 126:71–75

    Article  Google Scholar 

  54. Mutha PK, Haaland KY, Sainburg RL (2012) The effects of brain lateralization on motor control and adaptation. J Motor Behav 44:455–469

    Article  Google Scholar 

  55. Nepomnyashchikh VA, Izvekov EI (2006) Variability of the behavioural laterality in Teleostei (Pisces). J Ichthyology 46:235–242

    Article  Google Scholar 

  56. Patton P, Windsor S, Coombs S (2010) Active wall following by Mexican blind cavefish (Astyanax mexicanus). J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196(11):853–867. https://doi.org/10.1007/s00359-010-0567-8

    Article  PubMed  Google Scholar 

  57. Pongrácz P, Miklósi A, Kubinyi E, Gurobi K, Topál J, Csányi V (2001) Social learning in dogs: the effect of a human demonstrator on the performance of dogs in a detour task. Anim Behav 62:1109–1117

    Article  Google Scholar 

  58. Prior H, Wiltschko R, Stapput K, Güntürkün O, Wiltschko W (2004) Visual lateralization and homing in pigeons. Behav Brain Res 154(2):301–310

    PubMed  Article  Google Scholar 

  59. Reddon AR, Hurd PL (2009) Sex differences in the cerebral lateralization of a cichlid fish when detouring to view emotionally conditioned stimuli. Behav Process 82:25–29

    Article  Google Scholar 

  60. Regolin L, Vallortigara G, Zanforlin M (1995) Detour behaviour in the domestic chick: searching for a disappearing prey or a disappearing social partner. Anim Behav 50:203–211

    Article  Google Scholar 

  61. Rigosi E, Haase A, Rath L, Anfora G, Vallortigara G, Szyszka P (2015) Asymmetric neural coding revealed by in vivo calcium imaging in the honey bee brain. Proc R Soc B 282:20142571

    PubMed  Article  PubMed Central  Google Scholar 

  62. Robins A, Rogers L (2004) Lateralised prey catching responses in the toad (Bufo marinus): Analysis of complex visual stimuli. Anim Behav 68:767–775

    Article  Google Scholar 

  63. Robins A, Chen P, Beazley LD, Dunlop SA (2005) Lateralized predatory responses in the ornate dragon lizard (Ctenophorus ornatus). NeuroReport 16:849–852

    PubMed  Article  PubMed Central  Google Scholar 

  64. Rogers LJ (2000) Evolution of hemispheric specialization: advantages and disadvantages. Brain Lang 73:236–253

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  65. Rogers LJ, Zucca P, Vallortigara G (2004) Advantages of having a lateralized brain. Proc R Soc B 271:420–422

    Article  Google Scholar 

  66. Rørvang MV, Ahrendt LP, Christensen JW (2015) Horses fail to use social learning when solving spatial detour tasks. Anim Cogn 18:847–854

    PubMed  Article  PubMed Central  Google Scholar 

  67. Schnell AK, Jozet-Alves C, Hall KC, Radday L, Hanlon RT (2019) Fighting and mating success in giant Australian cuttlefish is influenced by behavioural lateralization. Proc R Soc B 286:20182507

    PubMed  Article  PubMed Central  Google Scholar 

  68. Simon P, Dupuis R, Costentin J (1994) Thigmotaxis as an index of anxiety in mice. Influence of dopaminergic transmissions. Behav Brain Res 61(1):59–64. https://doi.org/10.1016/0166-4328(94)90008-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  69. Sovrano VA (2004) Visual lateralization in response to familiar and unfamiliar stimuli in fish. Behav Brain Res 152:385–391

    PubMed  Article  Google Scholar 

  70. Sovrano VA (2007) A note on asymmetric use of the forelimbs during feeding in the European green toad (Bufo viridis). Laterality 12:458–463

    PubMed  Article  Google Scholar 

  71. Sovrano VA, Dadda M, Bisazza A (2005) Lateralized fish perform better than nonlateralized fish in spatial reorientation tasks. Behav Brain Res 163:122–127

    PubMed  Article  Google Scholar 

  72. Sovrano VA, Quaresmini C, Stancher G (2018) Tortoises in front of mirrors: Brain asymmetries and lateralized behaviours in the tortoise (Testudo hermanni). Behav Brain Res 352:183–186

    PubMed  Article  Google Scholar 

  73. Stier A, Geange S, Bolker B (2013) Predator density and competition modify the benefits of group formation in a shoaling reef fish. Oikos 122:171–178

    Article  Google Scholar 

  74. Stoffel MA, Nakagawa S, Schielzeth H (2017) rptR: repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol Evol 8:1639–1644

    Article  Google Scholar 

  75. Takeuchi Y, Hori M, Oda Y (2012) Lateralized kinematics of predation behaviour in a Lake Tanganyika scale-eating cichlid fish. PLoS ONE 7:29272

    Article  CAS  Google Scholar 

  76. Taylor R, Hsieh YW, Gamse J, Chuang CF (2010) Making a difference together: Reciprocal interactions in C. elegans and zebrafish asymmetric neural development. Development 137:681–691

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  77. Torres-Dowdall J, Rometsch SJ, Aguilera G, Goyenola G, Meyer A (2020) Asymmetry in genitalia is in sync with lateralized mating behaviour but not with the lateralization of other behaviours. Curr Zool 66:71–81

    PubMed  Article  Google Scholar 

  78. Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–589

    PubMed  Article  PubMed Central  Google Scholar 

  79. Vallortigara G, Regolin L, Pagni P (1999) Detour behaviour, imprinting and visual lateralization in the domestic chick. Cogn Brain Res 7:307–320

    CAS  Article  Google Scholar 

  80. Vallortigara G, Chiandetti C, Sovrano VA (2011) Brain asymmetry (animal). Wiley Interdiscip Rev Cogn Sci 2:146–157

    PubMed  Article  Google Scholar 

  81. Versace E, Morgante M, Pulina G, Vallortigara G (2007) Behavioural lateralization in sheep (Ovis aries). Behav Brain Res 184:72–80

    PubMed  Article  Google Scholar 

  82. Ward AJW (2012) Social facilitation of exploration in mosquitofish (Gambusia holbrooki). Behav Ecol Sociobiol 66:223–230

    Article  Google Scholar 

  83. Wilzeck C, Wiltschko W, Güntürkün O, Wiltschko R, Prior H (2010) Lateralization of magnetic compass orientation in pigeons. J Roy Soc Interface 7:235–240

    Article  Google Scholar 

Download references

Acknowledgements

We thank the staff of ANU Animal Services for assistance with fish husbandry, and D. Roche for helpful comments on an early version of the manuscript.

Funding

The study was funded by the Australian Research Council (DP190100279 to MDJ).

Author information

Affiliations

Authors

Contributions

IMV, MDJ and RJF conceived and designed the study, IMV collected the data, IMV and TN analysed the data. All authors interpreted the data, co-wrote the manuscript and gave permission for publication.

Corresponding author

Correspondence to Ivan M. Vinogradov.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethical approval

All experimental procedures were carried out under approval from ANU Animal Ethics Committee (Approval #A2018/27) and complied with existing laws regulating the treatment of vertebrates in Australia. The collection of animals was conducted under a Scientific License from the Australian Capital Territory (ACT) Government, granted under Section 21 of the Fisheries Act 2000, license number FS20188.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Vinogradov, I.M., Jennions, M.D., Neeman, T. et al. Repeatability of lateralisation in mosquitofish Gambusia holbrooki despite evidence for turn alternation in detour tests. Anim Cogn (2021). https://doi.org/10.1007/s10071-021-01474-8

Download citation

Keywords

  • Behavioural laterality
  • Cerebral lateralisation
  • Cognition
  • Poeciliidae
  • T-maze test