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.
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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
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):462–470
Bonati B, Csermely D, Romani R (2008) Lateralisation in the predatory behaviour of the common wall lizard (Podarcis muralis). Behav Proc 79(3):171–174
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):1–6
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):329–339
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):372–379
Cantalupo C, Bisazza A, Vallortigara G (1995) Lateralisation of predator-evasion response in a teleost fish (Girardinus falcatus). Neuropsychologia 33(12):1637–1646
Casteel DB (1911) The discriminative ability of the painted turtle. J Anim Behav 1(1)
Csermely D, Bonati B, Romani R (2010) Lateralisation in a detour test in the common wall lizard (Podarcis muralis). Laterality 15(5):535–547
Davey G (1989) Ecological learning theory. Routledge, London
Day LB, Crews D, Wilczynski W (1999) Spatial and reversal learning in congeneric lizards with different foraging strategies. Anim Behav 57(2):393–407
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):440
Deckel AW (1995) Laterality of aggressive responses in Anolis. J Exp Zool Part A Ecol Genet Physiol 272(3):194–200
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 555–579
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):229–234
Fagot J, Vauclair J (1988a) Handedness and bimanual coordination in the lowland gorilla. Brain Behav Evol 32:89–95
Fagot J, Vauclair J (1988b) Handedness and manual specialization in the baboon. Neuropsychologia 26:795–804
Fox K (2003) Effect displays in R for generalised linear models. J Stat Softw 8(15):1–27. http://www.jstatsoft.org/v08/i15/
Franklin WE, Lima SL (2001) Laterality in avian vigilance: do sparrows have a favourite eye? Anim Behav 62(5):879–885
Gaalema DE (2011) Visual discrimination and reversal learning in rough-necked monitor lizards. J Comp Psychol 125(2):246–249
Gans C, Gaunt AS, Webb PW (2011) Vertebrate Locomotion. Comprehensive physiology, Supplement 30: Handbook of Physiology, Comparative Physiology: 55–213. First published in print 1997
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):1079–1081
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):1–30
Holmes PA, Bitterman ME (1966) Spatial and visual habit reversal in the turtle. J Comp Physiol Psychol 62(2):328
Hopkins WD (1995) Hand preferences for a coordinated bimanual task in 110 chimpanzees (Pan troglodytes): cross-sectional analysis. J Comp Psychol 109(3):291
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):267–277
Jayes AS, McNeil Alexander R (1980) The gaits of chelonians: walking techniques for very low speeds. J Zool 191:353–378
Leal M, Powell BJ (2011) Behavioural flexibility and problem-solving in a tropical lizard. Biol Lett rsbl20110480
Lehman RA (1980) Distribution and changes in strength of hand preference of cynomolgus monkeys. Brain Behav Evol 17(3):209–217
Liu Y, Day LB, Summers K, Burmeister SS (2016) Learning to learn: advanced behavioural flexibility in a poison frog. Anim Behav 111:167–172
Mackintosh NJ, Mcgonigle B, Holgate V (1968) Factors underlying improvement in serial reversal learning. Can J Psychol 22(2):85
MacPhail E (1982) Brain and intelligence in vertebrates. Oxford University Press, Oxford, pp 136–167
Magat M, Brown C (2009) Laterality enhances cognition in Australian parrots. Proc R Soc Lond B Biol Sci 276(1676):4155–4162
Marchant LF, Steklis HD (1986) Hand preference in a captive island group of chimpanzees (Pan troglodytes). Am J Primatol 10(4):301–313
Martin P, Bateson P (1986) Measuring animal behaviour: a laboratory guide. Cambridge University Press, Cambridge, 200 p
McGrew WC, Marchant LF (1999) Laterality of hand use pays off in foraging success for wild chimpanzees. Primates 40(3):509–513
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):638–645
Moskovits D, Bjorndal A (1990) Diet and food preferences of the tortoises Geochelone carbonaria and G. denticulata in Northwestern Brazil. Herpetologica 46(2):207–218
Piddington T, Rogers LJ (2013) Strength of hand preference and dual task performance by common marmosets. Anim Cognit 1–9
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
R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, https://www.R-project.org/
Rodriguez M, Gomez C, Alonso J, Afonso D (1992) Laterality, alternation, and perseveration relationships on the T-maze test. Behav Neurosci 106(6):974
Rogers LJ (2000) Evolution of hemispheric specialization: advantages and disadvantages. Brain Lang 73(2):236–253
Rogers LJ, Zucca P, Vallortigara G (2004) Advantages of having a lateralized brain. Proc R Soc Lond B Biol Sci 271(6):S420–S422
Smith E (2012) Can a tortoise learn to reverse? Testing the cognitive flexibility of the Red Footed tortoise (Geochelone carbonaria). Schildkröten im Fokus 5:1–18
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):30706–30704
Spigel IM (1963) Running speed and intermediate brightness discrimination in the fresh water turtle (Chrysemys). J Comp Physiol Psychol 56(5):924
Spigel IM (1966) Variability in maze-path selection by turtle. J Gen Psychol 75(1):21–27
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):183
Stancher G, Clara E, Regolin L, Vallortigara G (2006) Lateralized righting behavior in the tortoise (Testudo hermanni). Behav Brain Res 173(2):315–319
Tinklepaugh OL (1932) Maze learning of a turtle. J Comp Psychol 13(2):201
Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralisation. Behav Brain Sci 28(4):575–588
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):135–143
Vallortigara G, Rogers LJ, Bisazza A (1999) Possible evolutionary origins of cognitive brain lateralisation. Brain Res Rev 30(2):164–175
Vauclair J, Meguerditchian A, Hopkins WD (2005) Hand preferences for unimanual and coordinated bimanual tasks in baboons (Papio anubis). Cogn Brain Res 25(1):210–216
Wilkinson A, Huber L (2012) Cold-blooded cognition: reptilian cognitive abilities. Oxford Handb Compar Evolut Psychol 1–8
Wilkinson A, Coward S, Hall G (2009) Visual and response-based navigation in the tortoise (Geochelone carbonaria). Anim Cogn 12(6):779–787
Wilkinson A, Mueller-Paul J, Huber L (2013) Picture–object recognition in the tortoise Chelonoidis carbonaria. Anim Cogn 16(1):99–107
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York, p 574
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).
The research program supporting this study was funded by an NSERC Discovery Grant to GJT (RGPIN-2014-05814).
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Justin Bridgeman and Glenn Tattersall declare that they have no conflict of interest.
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Bridgeman, J.M., Tattersall, G.J. Tortoises develop and overcome position biases in a reversal learning task. Anim Cogn 22, 265–275 (2019). https://doi.org/10.1007/s10071-019-01243-8
- Reversal learning
- Position bias