The Ebbinghaus illusion in a fish (Xenotoca eiseni)

Abstract

The tendency of fish to perceive the Ebbinghaus illusion was investigated. Redtail splitfins (Xenotoca eiseni, family Goodeidae) were trained to discriminate between two disks of different sizes. Then, fish were presented with two disks of the same size surrounded by disks of large or small size (inducers) arranged to produce the impression (to a human observer) of two disks of different sizes (in the Ebbinghaus illusion, a central disk surrounded by small inducers appears bigger than an identical one surrounded by large inducers). Fish chose the stimulus that, on the basis of a perception of the Ebbinghaus illusion, appeared deceptively larger or smaller, consistent with the condition of training. These results demonstrate that redtail splitfins tend to perceive this particular illusion. The results are discussed with reference to other related illusions that have been recently observed to be experienced by fish (such as the Navon effect), and with regard to their possible evolutionary implications.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Aglioti S, DeSouza JF, Goodale MA (1995) Size-contrast illusions deceive the eye but not the hand. Curr Biol 5:679–685

    CAS  PubMed  Article  Google Scholar 

  2. Agrillo C, Miletto Petrazzini ME, Dadda M (2014) Illusory patterns are fishy for fish, too. Front Neural Circuits 7:137

    Google Scholar 

  3. Barbet I, Fagot J (2002) Perception of the corridor illusion by baboons (Papio papio). Behav Brain Res 132:111–115

    PubMed  Article  Google Scholar 

  4. Bayne K, Davis R (1983) Susceptibility of rhesus monkeys (Macaca mulatta) to the Ponzo illusion. Bull Psychon Soc 21:476–478

    Article  Google Scholar 

  5. Cavoto KK, Cook RG (2001) Cognitive precedence for local information in hierarchical stimulus processing by pigeons. J Exp Psychol Anim Behav Proc 27(1):3–16

    CAS  Article  Google Scholar 

  6. Cerella J (1980) The pigeon’s analysis of pictures. Pattern Recognit 12(1):1–6

    Article  Google Scholar 

  7. Chiandetti C, Pecchia T, Patt F, Vallortigara G (2014) Visual hierarchical processing and lateralization of cognitive functions through domestic chicks’ eyes. PLoS One 9(1):e84435

    PubMed Central  PubMed  Article  Google Scholar 

  8. Choplin JM, Medin DL (1999) Similarity of the perimeters in the Ebbinghaus illusion. Percept Psychophys 61:3–12

    CAS  PubMed  Article  Google Scholar 

  9. Cook RG (1992) Dimensional organization and texture discrimination in pigeons. J Exp Psychol Anim Behav Proc 18:354–363

    CAS  Article  Google Scholar 

  10. Cook RG, Cavoto KK, Cavoto BR (1996) Mechanisms of multidimensional grouping, fusion, and search. Anim Learn Behav 24:150–167

    Article  Google Scholar 

  11. Coren S, Enns JT (1993) Size contrast as a function of conceptual similarity between test and inducers. Percept Psychophys 54:579–588

    CAS  PubMed  Article  Google Scholar 

  12. Danckert JA, Sharif N, Haffenden AM, Schiff KC, Goodale MA (2002) A temporal analysis of grasping in the Ebbinghaus illusion: planning versus online control. Exp Brain Res 144:275–280

    PubMed  Article  Google Scholar 

  13. Darmaillacq AS, Dickel L, Rahmani N, Shashar N (2011) Do reef fish, Variola louti and Scarus niger, perform amodal completion? Evidence from a field study. J Comp Psychol 125:273

    PubMed  Article  Google Scholar 

  14. De Fockert J, Davidoff J, Fagot J, Parron C, Goldstein J (2007) More accurate size contrast judgments in the Ebbinghaus illusion by a remote culture. J Exp Psychol Hum Percept Perform 3:738–742

    Article  Google Scholar 

  15. De Grave DDJ, Biegstraaten M, Smeets JBJ, Brenner E (2005) Effects of the Ebbinghaus figure on grasping are not only due to misjudged size. Exp Brain Res 163:58–64

    PubMed  Article  Google Scholar 

  16. Deruelle C, Fagot J (1998) Visual search for global/local stimulus features in humans and baboons. Psychon Bull Rev 5:476–481

    Article  Google Scholar 

  17. Ebbinghaus H (1902) Grundzüge der psychologie. Veit, Leipzig

    Google Scholar 

  18. Fagot J, Deruelle C (1997) Processing of global and local visual information and hemispheric specialization in humans (Homo sapiens) and baboons (Papio papio). J Exp Psychol Hum Percept Perform 23:429–442

    CAS  PubMed  Article  Google Scholar 

  19. Forkman B, Vallortigara G (1999) Minimization of modal contours: an essential cross species strategy in disambiguating relative depth. Anim Cogn 4:181–185

    Article  Google Scholar 

  20. Fremouw T, Herbranson WT, Shimp CP (1998) Priming of attention to local and global levels of visual analysis. J Exp Psychol Anim Behav Proc 24:278–290

    CAS  Article  Google Scholar 

  21. Fremouw T, Herbranson WT, Shimp CP (2002) Dynamic shifts of pigeon local/global attention. Anim Cogn 5:233–243

    PubMed  Article  Google Scholar 

  22. Fujita K (1996) Linear perspective and the Ponzo illusion: a comparison between rhesus monkeys and humans. Jpn Psychol Res 38:136–145

    Article  Google Scholar 

  23. Fujita K (1997) Perception of the Ponzo illusion by rhesus monkeys, chimpanzees, and humans: similarity and difference in the three primate species. Percept Psychophys 59:284–292

    CAS  PubMed  Article  Google Scholar 

  24. Fujita K, Blough DS, Blough PM (1991) Pigeons see the Ponzo illusion. Anim Learn Behav 19:283–293

    Article  Google Scholar 

  25. Fujita K, Blough DS, Blough PM (1993) Effects of the inclination of context lines on perception of the Ponzo illusion by pigeons. Anim Learn Behav 21:29–34

    Article  Google Scholar 

  26. Fuss T, Bleckmann H, Schluessel V (2014) The brain creates illusions not just for us: sharks (Chiloscyllium griseum) can “see the magic” as well. Front Neural Circuits 20:8–24

    Google Scholar 

  27. Geiger G, Poggio T (1975) The Müller-Lyer figure and the fly. Science 190:479–480

    CAS  PubMed  Article  Google Scholar 

  28. Girgus JS, Coren S, Agdern M (1972) The interrelationship between the Ebbinghaus and Delboeuf illusions. J Exp Psychol 95:453–455

    CAS  PubMed  Article  Google Scholar 

  29. Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15:20–25

    CAS  PubMed  Article  Google Scholar 

  30. Happé F (1996) Studying weak central coherence at low levels: children with autism do not succumb to visual illusions. A research note. J Child Psychol Psychiatry 37:873–877

    PubMed  Article  Google Scholar 

  31. Horridge GA, Zang S-W, O’Carrol D (1992) Insect perception of illusory contours. Philos Trans R Soc Lond B 337:59–64

    Article  Google Scholar 

  32. Kaldy Z, Kovacs I (2003) Visual context integration is not fully developed in 4-year-old children. Perception 32:657–666

    PubMed  Article  Google Scholar 

  33. Kimchi R (1992) Primacy of wholistic processing and global/local paradigm: a critical review. Psychol Bull 112:24–38

    CAS  PubMed  Article  Google Scholar 

  34. Kinchla RA, Wolf JM (1979) The order of visual processing: top-down, bottom-up, or middle-out. Percept Psychophys 25:225–231

    CAS  PubMed  Article  Google Scholar 

  35. Kinchla RA, Solis-Macias V, Hoffman J (1983) Attending to different levels of structure in a visual image. Percept Psychophys 33:1–10

    CAS  PubMed  Article  Google Scholar 

  36. Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nature 392:917–920

    CAS  PubMed  Article  Google Scholar 

  37. Mascalzoni E, Regolin L (2011) Animal visual perception. Wiley Interdiscip Rev Cogn Sci 2:106–116

    Article  Google Scholar 

  38. Massaro DW, Anderson NH (1971) Judgemental model of the Ebbinghaus illusion. J Exp Psychol 89:147–151

    CAS  PubMed  Article  Google Scholar 

  39. Murayama T, Usui A, Takeda E, Kato K, Maejima K (2012) Relative size discrimination and perception of the Ebbinghaus illusion in a bottlenose dolphin (Tursiops truncatus). Aquat Mamm 38:333–342

    Article  Google Scholar 

  40. Nakamura N, Fujita K, Ushitani T, Miyata H (2006) Perception of the standard and the reversed Müller-Lyer figures in pigeons (Columba livia) and humans (Homo sapiens). J Comp Psychol 120:252–261

    PubMed  Article  Google Scholar 

  41. Nakamura N, Watanabe S, Fujita K (2008) Pigeons perceive the Ebbinghaus–Titchener circles as an assimilation illusion. J Exp Psychol Anim Behav Proc 34(3):375–387

    Article  Google Scholar 

  42. Nakamura N, Watanabe S, Fujita K (2009) Further analysis of perception of reversed Müller-Lyer figures for pigeons (Columba livia). Percept Mot Skills 108:239–250

    PubMed  Article  Google Scholar 

  43. Nakamura N, Watanabe S, Fujita K (2014) A reversed Ebbinghaus–Titchener illusion in bantams (Gallus gallus domesticus). Anim Cogn 17:471–481

    PubMed  Article  Google Scholar 

  44. Navon D (1977) Forest before trees: precedence of global features in visual perception. Cogn Psychol 9:353–383

    Article  Google Scholar 

  45. Oyama T (1960) Japanese studies on the so-called geometrical-optical illusions. Psychologia 3:7–20

    Google Scholar 

  46. Parron C, Fagot J (2007) Comparison of grouping abilities in humans (Homo sapiens) and baboons (Papio papio) with Ebbinghaus illusion. J Comp Psychol 121:405–411

    PubMed  Article  Google Scholar 

  47. Pepperberg IM, Vicinay J, Cavanagh P (2008) Processing of the Müller-Lyer illusion by a grey parrot (Psittacus erithacus). Perception 37:765–781

    PubMed  Article  Google Scholar 

  48. Phillips WA, Chapman KL, Berry PD (2004) Size perception is less context sensitive in males. Perception 33:79–86

    PubMed  Article  Google Scholar 

  49. Pomerantz JR (1983) Global and local precedence: selective attention in form and motion perception. J Exp Psychol Gen 112:516–540

    CAS  PubMed  Article  Google Scholar 

  50. Regolin L, Vallortigara G (1995) Perception of partly occluded objects by young chicks. Percept Psychophys 57:971–976

    CAS  PubMed  Article  Google Scholar 

  51. Regolin L, Marconato F, Vallortigara G (2004) Hemispheric differences in the recognition of partly occluded objects by newly-hatched domestic chicks (Gallus gallus). Anim Cogn 7:162–170

    PubMed  Article  Google Scholar 

  52. Reiner A, Yamamoto K, Karten HJ (2005) Organization and evolution of the avian forebrain. Anat Rec A Discov Mol Cell Evol Biol 287A:1080–1120

    Article  Google Scholar 

  53. Roberts B, Harris MG, Yates TA (2005) The roles of inducer size and distance in the Ebbinghaus illusion (Titchener circle). Perception 34:847–856

    PubMed  Article  Google Scholar 

  54. Robertson LC, Egly R, Lamb MR, Kerth L (1993) Spatial attention and cuing to global and local levels of hierarchical structure. J Exp Psychol Hum Percept Perform 19:471–487

    CAS  PubMed  Article  Google Scholar 

  55. Rosa Salva O, Rugani R, Cavazzana A, Regolin L, Vallortigra G (2013) Perception of the Ebbinghaus illusion in four-day-old domestic chicks (Gallus gallus). Anim Cogn 16:895–906

    CAS  PubMed  Article  Google Scholar 

  56. Rosa Salva O, Sovrano VA, Vallortigara G (2014) What can fish brains tell us about visual perception. Front Neural Circuits 8:119. doi:10.3389/fncir.2014.00119

    PubMed Central  PubMed  Article  Google Scholar 

  57. Shimizu T (2004) Comparative cognition and neuroscience: misconceptions about brain evolution. Jpn Psychol Res 46:246–254

    Article  Google Scholar 

  58. Shimizu T, Bowers AN (1999) Visual circuits of the avian telencephalon: evolutionary implications. Behav Brain Res 98:183–191

    CAS  PubMed  Article  Google Scholar 

  59. Sovrano VA, Bisazza A (2008) Recognition of partly occluded objects by fish. Anim Cogn 11:161–166

    PubMed  Article  Google Scholar 

  60. Sovrano VA, Bisazza A (2009) Perception of subjective contours in fish. Perception 38:579–590

    PubMed  Article  Google Scholar 

  61. Steinke D, Salzburger W, Meyer A (2006) Novel relationships among ten fish model species revealed based on a phylogenomic analysis using ESTs. J Mol Evol 62:772–784

    CAS  PubMed  Article  Google Scholar 

  62. Suganuma E, Pessoa VF, Monge-Fuentes V, Castro BM, Tavares MCH (2007) Perception of the Müller-Lyer illusion in capuchin monkeys (Cebus apella). Behav Brain Res 182:67–72

    PubMed  Article  Google Scholar 

  63. Sutherland NS, Mackintosh NJ (1971) Mechanisms of animal discrimination learning. Academic Press, London

    Google Scholar 

  64. Timney B, Keil K (1996) Horses are sensitive to pictorial depth cues. Perception 25:1121–1128

    CAS  PubMed  Article  Google Scholar 

  65. Truppa V, Sovrano VA, Spinozzi G, Bisazza A (2010) Processing of visual hierarchical stimuli by fish (Xenoteca eiseni). Behav Brain Res 207(1):51–60

    PubMed  Article  Google Scholar 

  66. Tudusciuc O, Nieder A (2010) Comparison of length judgments and the Müller-Lyer illusion in monkeys and humans. Exp Brain Res 207:221–231

    PubMed  Article  Google Scholar 

  67. Ushitani T, Fujita K, Yamanaka R (2001) Do pigeons (Columba livia) perceive object unity? Anim Cogn 4:153–161

    CAS  PubMed  Article  Google Scholar 

  68. Vallortigara G (2004) Visual cognition and representation in birds and primates. In: Rogers LJ, Kaplan G (eds) Vertebrate comparative cognition: are primates superior to non-primates?. Kluwer Academic/Plenum Publishers, New York, pp 57–94

    Google Scholar 

  69. Vallortigara G (2006) The cognitive chicken: visual and spatial cognition in a non-mammalian brain. In: Wasserman EA, Zentall TR (eds) Comparative cognition: experimental explorations of animal intelligence. Oxford University Press, Oxford, pp 41–58

    Google Scholar 

  70. Vallortigara G (2009) Original knowledge and the two cultures. In: Carafoli E, Danieli GA, Longo GO (eds) The two cultures: shared problems. Springer, Berlin, pp 125–145

    Google Scholar 

  71. Vallortigara G (2012) Core knowledge of object, number, and geometry: a comparative and neural approach. Cogn Neuropsychol 29:213–236

    PubMed  Article  Google Scholar 

  72. Vallortigara G, Chiandetti C, Rugani R, Sovrano VA, Regolin L (2010) Animal cognition. Wiley Interdiscip Rev Cogn Sci 1:882–893

    Article  Google Scholar 

  73. Wade NJ (2005) Perception and illusions, historical perspectives. Springer, Dordrecht

    Google Scholar 

  74. Wade NJ (2010) Visual illusions. Corsini encyclopedia of psychology. Wiley, Hoboken, pp 1–2

    Google Scholar 

  75. Warden CJ, Baar J (1929) The Müller-Lyer illusion in the ring dove, Turtur risorius. J Comp Psychol 9(4):275–292

    Article  Google Scholar 

  76. Wasserman EA, Kirkpatrick-Steger K, Van Hamme LJ, Biederman I (1993) Pigeons are sensitive to the spatial organization of complex visual stimuli. Psychol Sci 4:336–341

    Article  Google Scholar 

  77. Weintraub DJ (1979) Ebbinghaus illusion: context, contour, and age influence the judged size of a circle admist circles. J Exp Psychol Hum Percept Perform 5:353–364

    CAS  PubMed  Article  Google Scholar 

  78. Winslow CN (1933) Visual illusions in the chick. Arch Physiol 153:1–83

    Google Scholar 

  79. Wyzisk K (2005) Experimente zur Form- und Größenwahrnehmung beim Goldfisch (Carassius auratus) unter Verwendung von Scheinkonturen und Größentäuschungen. Ph.D. thesis, Johannes-Gutenberg-Universität Mainz, Germany

  80. Wyzisk K, Neumeyer C (2007) Perception of illusory surfaces and contours in goldfish. Vis Neurosci 24:291–298

    PubMed  Article  Google Scholar 

  81. Yamazaki Y, Otsuka Y, Kanazawa S, Yamaguchi MK (2010) Perception of the Ebbinghaus illusion in 5-to-8-month-old infants. Jpn Psychol Res 52(1):33–40

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by research grant from the Cassa di Risparmio of Trento e Rovereto. We wish to thank Matteo Kettmaier for his help with the experiments and Francesco Cerri for the maintenance of the aquaria.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standard

The experiments reported here comply with the current Italian and European Community laws for the ethical treatment of animals.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Valeria Anna Sovrano.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sovrano, V.A., Albertazzi, L. & Rosa Salva, O. The Ebbinghaus illusion in a fish (Xenotoca eiseni). Anim Cogn 18, 533–542 (2015). https://doi.org/10.1007/s10071-014-0821-5

Download citation

Keywords

  • Visual perception
  • Visual illusions
  • Ebbinghaus illusion
  • Titchener circles
  • Fish