Serial reversal learning in freshwater stingrays (Potamotrygon motoro)

  • Martha M. M. Daniel
  • Vera SchluesselEmail author
Original Paper


Serial reversal learning is considered a reliable approach for the testing of behavioral flexibility, and animals that inhabit fluctuating habitats and different environments are expected to possess behavioral and cognitive flexibility. The ocellate river stingray (Potamotrygon motoro) is one such species. Comprising the first serial reversal learning experiment among elasmobranchs, this study trained seven juvenile P. motoro in a visual two-alternative forced-choice task, in which a food-rewarded stimulus and an unrewarded alternative stimulus were presented in pseudo-random order on either side of a barrier. In the session after a stingray reached the learning criterion (LC), food was associated with the alternative stimulus, and this reward association continued to be switched whenever LC was achieved. Overall, five stingrays reversed successfully at least once. All of them required more sessions (mean = 67.8 sessions) for the first reversal than they needed during training (mean = 22 sessions). One stingray demonstrated progressive improvement across four reversal phases, thus showing that Potamotrygon motoro can inhibit a previously learned association faster with experience, probably as it develops strategies for rule identification. One individual became slower to reach the (LC) across three reversal phases, which may indicate a dominant influence of proactive interference. Another stingray demonstrated large fluctuations across three reversals. The fourth individual completed two reversals and required approximately the same number of sessions for each. One stingray had just completed one reversal by the end of this study. Since stingrays took longer than a related species to reverse learning, future studies could look at the effects of changing stimulus type or training regime on the performance of P. motoro.


Behavior Cognition Progressive improvement Vision Elasmobranch Learning 



We would like to sincerely thank Slawa Braun (animal caretaker, Institute of Zoology, University Bonn), for his availability regarding maintenance questions, repairs, and animal illness; Dr. Werner Ekau (Leibniz Center for Tropical Marine Research) for his insight and advice regarding statistics; and Dr. Ingolf Rick (Institute for Evolutionary Biology and Ecology), for helping obtain the visual spectra of the experimental stimuli.


No funding was provided for his study.

Compliance with ethical standards

Conflict of interest

Author Vera Schluessel declares that she has no conflict of interest. Author Martha M.M. Daniel declares that she has no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.


  1. Alvermann L (2018) Amodale Vervollstaendigung und Visuelle Aufloesing beim Pfauenaugen stechrochen (Potamotrygon motoro). University of Bonn, Bachelor ThesisGoogle Scholar
  2. Bawolt M (2019) Vergleich unterschiedlicher Trainingsmethoden beim seriellen Umkehrlernen bei Pseudotropheus zebra. University of Bonn, Bachelor ThesisGoogle Scholar
  3. Behar I, LeBedda JM II (1974) Effects of differential pretraining on learning-set formation in Rhesus monkeys. J Comp Physiol Psych 87(2):277–283CrossRefGoogle Scholar
  4. Behrend ER, Domesick VB, Bitterman ME (1965) Habit reversal in the fish. J Comp Physiol Psych 60(3):407–411CrossRefGoogle Scholar
  5. Biehn, J (2019) Visuelle Diskriminierung und serielles Umkehrlernen bei der Weißbauch schnappschildkröte. University of Bonn, Bachelor ThesisGoogle Scholar
  6. Bitterman ME (1965) Phyletic differences in learning. Amer. Psychologist 20:396–410CrossRefGoogle Scholar
  7. Bond AB, Kamil A, Balda RP (2007) Serial reversal learning and the evolution of behavioral flexibility in three species of North American Corvids (Gymnorhinus cyanocephalus, Nucifraga columbiana, Aphelocoma californica). J Comp Psychol 121(4):372–379PubMedCrossRefGoogle Scholar
  8. Bridgeman JM, Tattersall GJ (2019) Tortoises develop and overcome position biases in a reversal learning task. Anim Cogn 22:265–275PubMedCrossRefGoogle Scholar
  9. Broglio C, Rodríguez F, Gómez A, Arias JL, Salas C (2010) Selective involvement of the goldfish lateral pallium in spatial memory. Behav Brain Res 210:191–201PubMedCrossRefGoogle Scholar
  10. Buechel SD, Boussard A, Kotrschal A, van der Bijl W, Kolm N (2018) Brain size affects performance in a reversal-learning test. Proc R Soc B 285:20172031PubMedCrossRefGoogle Scholar
  11. Chase AR (2001) Music discriminations by carp (Cyprinus carpio). Anim Learn Behav 29(4):336–353CrossRefGoogle Scholar
  12. Christofzik N (2016) Visuelle Wahrnehmung und Diskriminierung numerischer Informationen beim Pfauenaugenstechrochen (Potamotrygon motoro). University of Bonn, Bachelo ThesisGoogle Scholar
  13. Cox PM, Harris PP, Huntingford C, Betts RA, Collins M, Jones CD, Jupp TE, Marengo JA, Nobre CA (2008) Increasing risk of Amazonian drought due to decreasing aerosol pollution. Nature 453:212–215PubMedCrossRefGoogle Scholar
  14. Datta LEG, Milstein S, Bitterman ME (1960) Habit reversal in the crab. J Comp Physiol Psychol 53:275–278PubMedCrossRefGoogle Scholar
  15. de Ramos AM, Zou Y, Oliveira GS, Kurths J, Macau EEN (2017) Unveiling non-stationary coupling between Amazon and ocean during recent extreme events. Clim Dyn 50:767–776CrossRefGoogle Scholar
  16. Duncan WP, Fernandes MN (2010) Physicochemical characterization of the white, black, and clearwater rivers of the Amazon Basin and its implications on the distribution of freshwater stingrays (Chondrichthyes, Potamotrygonidae). Pan-Am J Aquat Sci 5(3):454–464Google Scholar
  17. Engelhardt F, Woodard WT, Bitterman ME (1973) Discrimination reversal in the goldfish as a function of training conditions. J Comp Physiol Psychol 85(1):144–150CrossRefGoogle Scholar
  18. Evans BI (2004) A fish’s eye view of habitat change. In: von der Emde G, Mogdans J, Kapoor BG (eds) The senses of fish: adaptations for the reception of natural stimuli. Narosa Publishing House, New Delhi, pp 1–30Google Scholar
  19. Frank AH, Flood NB, Overmeier JB (1972) Reversal learning in forebrain ablated and olfactory tract sectioned teleost, Carassius auratus. Psychon Sci 26(3):149–151CrossRefGoogle Scholar
  20. Fuss T, Bleckmann H, Schluessel V (2014) Visual discrimination abilities in the gray bamboo shark (Chiloscyllium griseum). Zoology 117:104–111PubMedCrossRefGoogle Scholar
  21. Garrone Neto D, Uieda VS (2012) Activity and habitat use of two species of stingrays (Myliobatiformes: Potamotrygonidae) in the upper Paraná River basin, Southeastern Brazil. Neotrop Ichthyol 10(1):81–88CrossRefGoogle Scholar
  22. Gatling FP (1952) The effect of repeated stimulus-reversals on learning in the rat. J Comp Physiol Psychol 45:347–351PubMedCrossRefGoogle Scholar
  23. Goarin EHF, Lingawi NW, Laurent V (2018) Role played by the passage of time in reversal learning. Front Behav Neurosci 12(75):1–15Google Scholar
  24. Godfrey-Smith P (2002) Environmental complexity and the evolution of cognition. In: Sternberg R, Kaufman J (eds) The evolution of intelligence. Erlbaum, Mahwah, pp 233–249Google Scholar
  25. Gonzalez RC, Behrend ER, Bitterman ME (1967) Reversal learning and forgetting in bird and fish. Science 158:519–521PubMedCrossRefGoogle Scholar
  26. Henrichfreise G, Ducker G (1983) Vergleichende Untersuchungen zum Problem des serialen Umkehrlernens bei Fishen (Carassius auratus L., Cyprinus carpio L., Salmo gairdneri Richardson). Zoologischer Anzeiger 211(3–4):197–213Google Scholar
  27. John L (2017) Konzeptlernen bei Pseudotropheus zebra: räumliche Anordnung versus Unterschiedlichkeit visueller Stimuli. University of Bonn, Bachelor ThesisGoogle Scholar
  28. Junk WJ, Bayley PB, Sparks RE (1989) The flood pulse concept in river-floodplain systems. In: Dodge DP (ed) Proc. Int. Large River Symp (Lars). Can Spec Publ Fish Aquat Sci 106:110–127Google Scholar
  29. Kuba MJ, Byrne RA, Burghardt GM (2010) A new method for studying problem solving and tool use in stingrays (Potamotrygon castexi). Anim Cogn 13:507–513PubMedCrossRefGoogle Scholar
  30. LaClair M, Lacreuse A (2016) Reversal learning in gonadectomized marmosets with and without hormone replacement: are males more sensitive to punishment? Anim Cogn 19(3):619–630PubMedPubMedCentralCrossRefGoogle Scholar
  31. Leal M, Powell BJ (2012) Behavioural flexibility and problem-solving in a tropical lizard. Biol Lett 8:28–30PubMedCrossRefGoogle Scholar
  32. Leo V (2019) Serieles Umkehrlernen beim Grauen Bambooshai (Chiloscyllium griseum). University of Bonn, Bachelor ThesisGoogle Scholar
  33. Loboda TS (2010) Revisão taxonômica e morfológica de Potamotrygon motoro (Müller & Henle, 1841) na bacia Amazônica (Chondrichthyes: Myliobatiformes: Potamotrygonidae). Dissertation, Universidade de São PauloGoogle Scholar
  34. López JC, Broglio C, Rodríguez F, Thinus-Blanc C, Salas C (1999) Multiple spatial learning strategies in goldfish (Carassius auratus). Anim Cogn 2:109–120CrossRefGoogle Scholar
  35. Lucon-Xiccato T, Bisazza A (2014) Discrimination reversal learning reveals greater female behavioral flexibility in guppies. Biol Lett 10:20140206PubMedCentralCrossRefPubMedGoogle Scholar
  36. Lui Y, Day LB, Summers K, Burmeister SS (2016) Learning to learn: advanced behavioural flexibility in a poison frog. Anim Behav 111:167–172CrossRefGoogle Scholar
  37. Mackintosh NJ, Cauty A (1971) Spatial reversal learning in rats, pigeons, and goldfish. Psychon Sci 22(5):281–282CrossRefGoogle Scholar
  38. Mackintosh NJ, Mcgonigle B, Holgate V (1968) Factors underlying improvement in serial reversal learning. Can J Psychol/Revue Canadienne de Psychologie 22(2):85–95CrossRefGoogle Scholar
  39. Mattioli R, Santangelo EM, Costa ACC, Vasconcelos L (1997) Substance P facilitates memory in goldfish in an appetitively motivated learning task. Behav Brain Res 85:117–120PubMedCrossRefGoogle Scholar
  40. Milner AD, Ettlinger G (1970) Cross-modal transfer of serial reversal learning in the monkey. Neuropsychologia 8:251–258PubMedCrossRefGoogle Scholar
  41. Mininni CJ, Zanutto BS (2017) Exploring the limits of learning: Segregation of information integration and response selection is required for learning a serial reversal task. PLoS One 12(10):1–26CrossRefGoogle Scholar
  42. Munger EL, Takemoto A, Raghantia MA, Nakamura K (2017) Visual discrimination and reversal learning in aged common marmosets (Callithrix jacchus). Neurosci Res 124:57–62PubMedCrossRefGoogle Scholar
  43. Parker MO, Gaviria J, Haigh A, Millington ME, Brown VJ, Combe FJ, Brennan CH (2012) Discrimination reversal and attention sets in zebrafish (Danio rerio). Behav Brain Res 232(1):264–268PubMedPubMedCentralCrossRefGoogle Scholar
  44. Portavella M, Vargas JP (2005) Emotional and spatial learning in goldfish is dependent on different telencephalic pallial systems. Euro J Neurosci 21:2800–2806CrossRefGoogle Scholar
  45. Pubols BH Jr (1957) Successive discrimination reversal learning in the white rat: a comparison of two procedures. J Comp Physiol Psychol 50(3):319–322PubMedCrossRefGoogle Scholar
  46. Reader SM (2003) Innovation and social learning: individual variation and brain evolution. Anim Biol 53:147–158CrossRefGoogle Scholar
  47. Rosa RS (1985) A systematic revision of the South American freshwater stingrays (Chondrichthyes: Potamotrygonidae). Dissertation, College of William and MaryGoogle Scholar
  48. Rygula R, Walker SC, Clarke HF, Robbins TW, Roberts AC (2010) Differential contributions of the primate ventrolateral prefrontal and orbitofrontal cortex to serial reversal learning. J Neurosci 30(43):14552–14559PubMedPubMedCentralCrossRefGoogle Scholar
  49. Salas C, Broglio C, Rodríguez F, López JC, Portavella M, Torres B (1996) Telencephalic ablation in goldfish impairs performance in a spatial constancy problem but not in a cued one. Behav Brain Res 79:193–200PubMedCrossRefGoogle Scholar
  50. Sánchez Duarte P, Lasso C, Ortiz-Arroyave LM, Morales-Betancourt MA, Loboda TS,Carvalho MR, Acosta-santos A, Agudelo-Cordoba E, Bonilla-Castillo CA, Gomez-Hurtado GA, Barriga R, Ortega H (2014) Familia Potamotrygonidae - Potamotrygon motoro_ Cuenca del Amazonas. In: Lasso CA, Rosa RS, Sánchez-Duarte P, Morales-Betancourt MA, Agudelo-Córdoba E, orgs. Rayas de Agua Dulce (Potamotrygonidae) de Suramérica, vol 1, pp 218–223Google Scholar
  51. Satyamurty P, Costa CPW, Manzi AO (2013) Moisture source for the Amazon Basin: a study of contrasting years. Theor Appl Climatol 111:195–209CrossRefGoogle Scholar
  52. Schluessel V, Bleckmann H (2005) Spatial memory and orientation strategies in the elasmobranch Potamotrygon motoro. J Comp Physiol 191:695–706CrossRefGoogle Scholar
  53. Schluessel V, Ober C (2018) How to get out of a maze? Stingrays (Potamotrygon motoro) use directional over landmark information when provided with both in a spatial task. Evol Ecol Res 19:619–637Google Scholar
  54. Schluessel V, Herzog H, Scherpenstein M (2015) Seeing the forest before the trees—spatial orientation in freshwater stingrays (Potamotrygon motoro) in a hole-board task. Behav Process 119:105–115CrossRefGoogle Scholar
  55. Seidman E (1949) Relative ability of the newt and the terrapin to reverse a direction habit. J Comp Physiol Psychol 42(5):320–327PubMedCrossRefGoogle Scholar
  56. Seifert FD (2017) Farbwahrnehmung beim Pfauenaugenstechrochen (Potamotrygon motoro). University of Bonn, Bachelor ThesisGoogle Scholar
  57. Sena JA, Deus LAB, Freitas MAV, Costa L (2012) Extreme events of droughts and floods in Amazonia: 2005 and 2009. Water Resour Manag 26:1665–1676CrossRefGoogle Scholar
  58. Sherry DF, Strang CG (2014) Serial reversal learning in bumblebees (Bombus impatiens). Anim Cogn 17:723–734PubMedCrossRefGoogle Scholar
  59. Shettleworth SJ (2010) Cognition, evolution, and behavior, 2nd edn. Oxford University Press, New YorkGoogle Scholar
  60. Thompson R (1957) Successive reversal of a position habit in an invertebrate. Science 126:163–164PubMedCrossRefGoogle Scholar
  61. Thonhauser KE, Gutnick T, Byrne RA, Kral K, Burghardt GM, Kuba MJ (2013) Social learning in Cartilaginous fish (stingrays Potamotrygon falkneri). Anim Cogn 16:927–932PubMedCrossRefGoogle Scholar
  62. Warren JM (1960) Reversal learning by paradise fish (Macropodus opercularis). J Comp Physiol Psychol 53(4):376–378PubMedCrossRefGoogle Scholar
  63. Warren JM, Brookshire KH, Ball GG, Reynolds DV (1960) Reversal learning by white leghorn chicks. J Comp Physiol Psychol 53(4):371–375PubMedCrossRefGoogle Scholar
  64. Wells MC, Lehner PN (1977) Serial reversal learning in the mallard duck (Anas platyrhynchos). Bull Psychon Soc 10(3):235–237CrossRefGoogle Scholar
  65. Wodinsky J, Bitterman ME (1957) Discrimination-reversal in the fish. Amer J Psychol 70(4):569–576PubMedCrossRefGoogle Scholar
  66. Young JZ (1962) Repeated reversal of training in octopus. Quart J Exp Psychol 14(4):206–222CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of ZoologyRheinische Friedrich-Wilhelms-Universität BonnBonnGermany

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