Advertisement

Animal Cognition

, Volume 22, Issue 2, pp 265–275 | Cite as

Tortoises develop and overcome position biases in a reversal learning task

  • Justin M. Bridgeman
  • Glenn J. TattersallEmail author
Original Paper

Abstract

The capability of animals to alter their behaviour in response to novel or familiar stimuli, or behavioural flexibility, is strongly associated with their ability to learn in novel environments. Reptiles are capable of learning complex tasks and offer a unique opportunity to study the relationship between visual proficiency and behavioural flexibility. The focus of this study was to investigate the behavioural flexibility of red-footed tortoises and their ability to perform reversal learning. Reversal learning involves learning a particular discrimination task, after which the previously rewarded cue is reversed and then subjects perform the task with new reward contingencies. Red-footed tortoises were required to learn to recognise and approach visual cues within a Y-maze. Once subjects learned the visual discrimination, tortoises were required to successfully learn four reversals. Tortoises required significantly more trials to reach criterion (80% correct) in the first reversal, indicating the difficulty of unlearning the positive stimulus presented during training. Nevertheless, subsequent reversals required a similar number of sessions to the training stage, demonstrating that reversal learning improved up to a point. All subjects tested developed a position bias within the Y-maze that was absent prior to training, but most were able to exhibit reversal learning. Red-footed tortoises primarily adopted a win-stay choice strategy while learning the discrimination without much evidence for a lose-shift choice strategy, which may explain limits to their behavioural flexibility. However, improving performance across reversals while simultaneously overcoming a position bias provides insights into the cognitive abilities of tortoises.

Keywords

Reptile Reversal learning Lateralisation Position bias Tortoise 

Notes

Acknowledgements

We would like to thank Tom Eles for the assistance with animal care, Dr. Cheryl McCormick for the scientific discussions during the course of this study, and Dr. Miriam Richards and Brock University’s Animal Behaviour class of 2014–2015 for assistance with pilot data collection on tortoise behaviour. This research was supported by a Natural Sciences and Engineering Research Council of Canada Discovery Grant to GJT (RGPIN-2014-05814). Data are made available at the Brock University repository (http://hdl.handle.net/10464/13911).

Funding

The research program supporting this study was funded by an NSERC Discovery Grant to GJT (RGPIN-2014-05814).

Compliance with Ethical Standards

Conflict of interest

Justin Bridgeman and Glenn Tattersall declare that they have no conflict of interest.

Ethical approval

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

Supplementary material

10071_2019_1243_MOESM1_ESM.pdf (216 kb)
Supplementary material 1 (PDF 216 KB)

Supplementary material 2 (M4V 8233 KB)

Supplementary material 3 (M4V 5709 KB)

Supplementary material 4 (M4V 5760 KB)

Supplementary material 5 (M4V 5561 KB)

References

  1. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48.  https://doi.org/10.18637/jss.v067.i01 Google Scholar
  2. Bonati B, Csermely D (2011) Complementary lateralisation in the exploratory and predatory behaviour of the common wall lizard (Podarcis muralis). Later Asymmetries Body Brain Cognit 16(4):462–470Google Scholar
  3. Bonati B, Csermely D, Romani R (2008) Lateralisation in the predatory behaviour of the common wall lizard (Podarcis muralis). Behav Proc 79(3):171–174Google Scholar
  4. Bonati B, Csermely D, López P, Martín J (2010) Lateralisation in the escape behaviour of the common wall lizard (Podarcis muralis). Behav Brain Res 207(1):1–6Google Scholar
  5. Bonati B, Csermely D, Sovrano VA (2013) Looking at a predator with the left or right eye: asymmetry of response in lizards. Later Asymmetries Body Brain Cognition 18(3):329–339Google Scholar
  6. Bond AB, Kamil AC, Balda RP (2007) Serial reversal learning and the evolution of behavioral flexibility in three species of North American corvids. J Comp Psychol 121(4):372–379Google Scholar
  7. Cantalupo C, Bisazza A, Vallortigara G (1995) Lateralisation of predator-evasion response in a teleost fish (Girardinus falcatus). Neuropsychologia 33(12):1637–1646Google Scholar
  8. Casteel DB (1911) The discriminative ability of the painted turtle. J Anim Behav 1(1)Google Scholar
  9. Csermely D, Bonati B, Romani R (2010) Lateralisation in a detour test in the common wall lizard (Podarcis muralis). Laterality 15(5):535–547Google Scholar
  10. Davey G (1989) Ecological learning theory. Routledge, LondonGoogle Scholar
  11. Day LB, Crews D, Wilczynski W (1999) Spatial and reversal learning in congeneric lizards with different foraging strategies. Anim Behav 57(2):393–407Google Scholar
  12. Day LB, Ismail N, Wilczynski W (2003) Use of position and feature cues in discrimination learning by the Whiptail Lizard (Cnemidophorus inornatus). J Comp Psychol 117(4):440Google Scholar
  13. Deckel AW (1995) Laterality of aggressive responses in Anolis. J Exp Zool Part A Ecol Genet Physiol 272(3):194–200Google Scholar
  14. Delius JD, Delius JM (2006) Intelligences and brains: an evolutionary birds’ eye view. In: Wasserman EA, Zentall TR (eds) Comparative cognition. Oxford University Press, Oxford, pp 555–579Google Scholar
  15. Facchin L, Bisazza A, Vallortigara G (1999) What causes lateralisation of detour behavior in fish? Evidence for asymmetries in eye use. Behav Brain Res 103(2):229–234Google Scholar
  16. Fagot J, Vauclair J (1988a) Handedness and bimanual coordination in the lowland gorilla. Brain Behav Evol 32:89–95Google Scholar
  17. Fagot J, Vauclair J (1988b) Handedness and manual specialization in the baboon. Neuropsychologia 26:795–804Google Scholar
  18. Fox K (2003) Effect displays in R for generalised linear models. J Stat Softw 8(15):1–27. http://www.jstatsoft.org/v08/i15/
  19. Franklin WE, Lima SL (2001) Laterality in avian vigilance: do sparrows have a favourite eye? Anim Behav 62(5):879–885Google Scholar
  20. Gaalema DE (2011) Visual discrimination and reversal learning in rough-necked monitor lizards. J Comp Psychol 125(2):246–249Google Scholar
  21. Gans C, Gaunt AS, Webb PW (2011) Vertebrate Locomotion. Comprehensive physiology, Supplement 30: Handbook of Physiology, Comparative Physiology: 55–213. First published in print 1997Google Scholar
  22. Güntürkün O, Diekamp B, Manns M, Nottelmann F, Prior H, Schwarz A, Skiba M (2000) Asymmetry pays: visual lateralisation improves discrimination success in pigeons. Curr Biol 10(17):1079–1081Google Scholar
  23. Halekoh U, Højsgaard S (2014) A Kenward–Roger approximation and parametric bootstrap methods for tests in linear mixed models—the R package pbkrtest. J Stat Softw 59(9):1–30Google Scholar
  24. Holmes PA, Bitterman ME (1966) Spatial and visual habit reversal in the turtle. J Comp Physiol Psychol 62(2):328Google Scholar
  25. Hopkins WD (1995) Hand preferences for a coordinated bimanual task in 110 chimpanzees (Pan troglodytes): cross-sectional analysis. J Comp Psychol 109(3):291Google Scholar
  26. Hopkins DW, Rabinowitz DM (1997) Manual specialisation and tool use in captive chimpanzees (Pan troglodytes): the effect of unimanual and bimanual strategies on hand preference. Later Asymmetries Body Brain Cognit 2(3–4):267–277Google Scholar
  27. Jayes AS, McNeil Alexander R (1980) The gaits of chelonians: walking techniques for very low speeds. J Zool 191:353–378Google Scholar
  28. Leal M, Powell BJ (2011) Behavioural flexibility and problem-solving in a tropical lizard. Biol Lett rsbl20110480Google Scholar
  29. Lehman RA (1980) Distribution and changes in strength of hand preference of cynomolgus monkeys. Brain Behav Evol 17(3):209–217Google Scholar
  30. Liu Y, Day LB, Summers K, Burmeister SS (2016) Learning to learn: advanced behavioural flexibility in a poison frog. Anim Behav 111:167–172Google Scholar
  31. Mackintosh NJ, Mcgonigle B, Holgate V (1968) Factors underlying improvement in serial reversal learning. Can J Psychol 22(2):85Google Scholar
  32. MacPhail E (1982) Brain and intelligence in vertebrates. Oxford University Press, Oxford, pp 136–167Google Scholar
  33. Magat M, Brown C (2009) Laterality enhances cognition in Australian parrots. Proc R Soc Lond B Biol Sci 276(1676):4155–4162Google Scholar
  34. Marchant LF, Steklis HD (1986) Hand preference in a captive island group of chimpanzees (Pan troglodytes). Am J Primatol 10(4):301–313Google Scholar
  35. Martin P, Bateson P (1986) Measuring animal behaviour: a laboratory guide. Cambridge University Press, Cambridge, 200 pGoogle Scholar
  36. McGrew WC, Marchant LF (1999) Laterality of hand use pays off in foraging success for wild chimpanzees. Primates 40(3):509–513Google Scholar
  37. Meguerditchian A, Calcutt SE, Lonsdorf EV, Ross SR, Hopkins WD (2010) Brief communication: captive gorillas are right-handed for bimanual feeding. Am J Phys Anthropol 141(4):638–645Google Scholar
  38. Moskovits D, Bjorndal A (1990) Diet and food preferences of the tortoises Geochelone carbonaria and G. denticulata in Northwestern Brazil. Herpetologica 46(2):207–218Google Scholar
  39. Piddington T, Rogers LJ (2013) Strength of hand preference and dual task performance by common marmosets. Anim Cognit 1–9Google Scholar
  40. Pinheiro J, Bates D, DebRoy S, Sarkar D, Core Team R (2015) nlme: linear and nonlinear mixed effects models. R package version 3.1–122, http://CRAN.Rproject.org/package = nlme
  41. R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, https://www.R-project.org/
  42. Rodriguez M, Gomez C, Alonso J, Afonso D (1992) Laterality, alternation, and perseveration relationships on the T-maze test. Behav Neurosci 106(6):974Google Scholar
  43. Rogers LJ (2000) Evolution of hemispheric specialization: advantages and disadvantages. Brain Lang 73(2):236–253Google Scholar
  44. Rogers LJ, Zucca P, Vallortigara G (2004) Advantages of having a lateralized brain. Proc R Soc Lond B Biol Sci 271(6):S420–S422Google Scholar
  45. Smith E (2012) Can a tortoise learn to reverse? Testing the cognitive flexibility of the Red Footed tortoise (Geochelone carbonaria). Schildkröten im Fokus 5:1–18Google Scholar
  46. Sovrano VA, Quaresmini C, Stancher G (2017) Tortoises in front of mirrors: brain asymmetries and lateralized behaviours in the tortoise (Testudo hermanni). Behav Brain Res S0166–4328(17):30706–30704Google Scholar
  47. Spigel IM (1963) Running speed and intermediate brightness discrimination in the fresh water turtle (Chrysemys). J Comp Physiol Psychol 56(5):924Google Scholar
  48. Spigel IM (1966) Variability in maze-path selection by turtle. J Gen Psychol 75(1):21–27Google Scholar
  49. Spinozzi G, Castorina MG, Truppa V (1998) Hand preferences in unimanual and coordinated-bimanual tasks by tufted capuchin monkeys (Cebus apella). J Comp Psychol 112(2):183Google Scholar
  50. Stancher G, Clara E, Regolin L, Vallortigara G (2006) Lateralized righting behavior in the tortoise (Testudo hermanni). Behav Brain Res 173(2):315–319Google Scholar
  51. Tinklepaugh OL (1932) Maze learning of a turtle. J Comp Psychol 13(2):201Google Scholar
  52. Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralisation. Behav Brain Sci 28(4):575–588Google Scholar
  53. Vallortigara G, Regolin L, Bortolomiol G, Tommasi L (1996) Lateral asymmetries due to preferences in eye use during visual discrimination learning in chicks. Behav Brain Res 74(1):135–143Google Scholar
  54. Vallortigara G, Rogers LJ, Bisazza A (1999) Possible evolutionary origins of cognitive brain lateralisation. Brain Res Rev 30(2):164–175Google Scholar
  55. Vauclair J, Meguerditchian A, Hopkins WD (2005) Hand preferences for unimanual and coordinated bimanual tasks in baboons (Papio anubis). Cogn Brain Res 25(1):210–216Google Scholar
  56. Wilkinson A, Huber L (2012) Cold-blooded cognition: reptilian cognitive abilities. Oxford Handb Compar Evolut Psychol 1–8Google Scholar
  57. Wilkinson A, Coward S, Hall G (2009) Visual and response-based navigation in the tortoise (Geochelone carbonaria). Anim Cogn 12(6):779–787Google Scholar
  58. Wilkinson A, Mueller-Paul J, Huber L (2013) Picture–object recognition in the tortoise Chelonoidis carbonaria. Anim Cogn 16(1):99–107Google Scholar
  59. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York, p 574Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of Biological SciencesBrock UniversitySt. CatharinesCanada

Personalised recommendations