Behavioral Ecology and Sociobiology

, Volume 68, Issue 2, pp 239–247 | Cite as

Colour discrimination and associative learning in hatchling lizards incubated at ‘hot’ and ‘cold’ temperatures

  • Benjamin F. Clark
  • Joshua J. Amiel
  • Richard Shine
  • Daniel W. A. Noble
  • Martin J. WhitingEmail author
Original Paper


The ability of an animal to acquire, process and learn from information in their environment is thought to be fundamental to fitness. We currently have a poor understanding of the learning ability of young animals within the first few months of their life, the types of learning they use and the extent of their learning ability. Furthermore, an animal’s developmental environment, such as nest incubation temperature, may profoundly influence motor and cognitive skills. We first tested the ability of hatchling three-lined skinks (Bassiana duperreyi) incubated at ‘hot’ and ‘cold’ temperatures to solve an instrumental (motor) task before assessing their ability to learn colour associations in a multi-stage instrumental task, with a choice reversal. While 53 (88.3 %) lizards successfully completed the training phase, 14 (46.7 %) of the ‘hot’ incubated and none of the ‘cold’ incubated lizards successfully completed the instrumental task. Thirteen of these lizards rapidly learnt to discriminate colours, and this culminated in eight individuals successfully completing a choice reversal. Hatchling B. duperreyi demonstrated surprisingly rapid learning, and these results highlight the potentially important role of cognition during development and ultimately, in fitness.


Cognition Incubation Choice reversal Motor task 



Funding of this study was from Australian Research Council to RS, Natural Sciences and Engineering Research Council of Canada to JJA and DWAN, and a Macquarie University internal grant to BFC and MJW. We thank the reviewers for their constructive criticism of our study.

Ethical standards

All work was carried out under the approval of the Animal Ethics Committee of the University of Sydney (ARA 5361) in agreement with the Animal Ethics Committee of Macquarie University.


  1. Amiel JJ, Lindström T, Shine R (2013) Egg incubation effects generate positive correlations between size, speed and learning ability in young lizards. Anim Cogn. doi: 10.1007/s10071-013-0665-4 PubMedGoogle Scholar
  2. Amiel JJ, Shine R (2012) Hotter nests produce smarter young lizards. Biol Lett 8:372–374PubMedCentralPubMedCrossRefGoogle Scholar
  3. Burghardt GM (1977) Learning processes in reptiles. In: Gans C, Tinkle DW (eds) Biology of the Reptilia, vol 7, Ecology and Behaviour A. Academic Press, London, pp 555–681Google Scholar
  4. Chapillon P, Patin V, Roy V, Vincent A, Caston J (2002) Effects of pre- and postnatal stimulation on developmental, emotional, and cognitive aspects in rodents: A review. Dev Psychobiol 41:373–387Google Scholar
  5. Coomber P, Crews D, Gonzalez-Lima F (1997) Independent effects of incubation temperature and gonadal sex on the volume and metabolic capacity of brain nuclei in the leopard gecko (Eublepharis macularius), a lizard with temperature-dependent sex determination. J Comp Neurol 380:409–421PubMedCrossRefGoogle Scholar
  6. Cooper W, Greenberg N (1992) Reptilian coloration and behavior. Biol Reptil 18:298–422Google Scholar
  7. 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 117:440–448PubMedCrossRefGoogle Scholar
  8. Denenberg VH, Hoplight BJ, Mobraaten LE (1998) The uterine environment enhances cognitive competence. Neuroreport 9:1667–1671PubMedCrossRefGoogle Scholar
  9. Doody JS, Paull P (2013) Hitting the ground running: environmentally cued hatching in a lizard. Copeia 2013:160–165CrossRefGoogle Scholar
  10. Dubey S, Shine R (2010) Evolutionary diversification of the lizard genus Bassiana (Scincidae) across Southern Australia. PLoS ONE 5:e12982. doi: 10.1371/journal.pone.0012982 PubMedCentralPubMedCrossRefGoogle Scholar
  11. Dukas R (2009) Learning: mechanisms, ecology, and evolution. In: Dukas R, Ratcliffe JM (eds) Cognitive ecology II. Chicago University Press, Chicago, pp 7–26CrossRefGoogle Scholar
  12. Elphick MJ, Shine R (1998) Long-term effects of incubation temperatures on the morphology and locomotor performance of hatchling lizards (Bassiana duperreyi, Scincidae). Biol J Linn Soc 63:429–447CrossRefGoogle Scholar
  13. Fleishman LJ, Loew ER, Whiting MJ (2011) High sensitivity to short wavelengths in a lizard and implications for understanding the evolution of visual systems in lizards. Proc R Soc Lond B 278:2891–2899CrossRefGoogle Scholar
  14. Gobbo O, O’Mara S (2004) Impact of enriched-environment housing on brain-derived neurotrophic factor and on cognitive performance after a transient global ischemia. Behav Brain Res 152:231–241PubMedCrossRefGoogle Scholar
  15. Halpern M (1992) Nasal chemical senses in reptiles: structure and function. In: Gans C (ed) Biology of the Reptilia: hormones, brain, and behaviour, vol 18, Physiology E. Chicago University Press, Chicago, pp 423–523Google Scholar
  16. Harlow PS (1996) A harmless technique for sexing hatchling lizards. Herpetol Rev 27:71–72Google Scholar
  17. Jones JC, Helliwell P, Beekman M, Maleszka R, Oldroyd BP (2005) The effects of rearing temperature on developmental stability and learning and memory in the honey bee, Apis mellifera. J Comp Physiol A 191:1121–1129CrossRefGoogle Scholar
  18. LaDage L, Roth T, Cerjanic A, Sinervo B, Pravosudov V (2012) Spatial memory: are lizards really deficient? Biol Lett 8:939–941PubMedCentralPubMedCrossRefGoogle Scholar
  19. Leal M, Powell BJ (2012) Behavioural flexibility and problem-solving in a tropical lizard. Biol Lett 8:28–30PubMedCentralPubMedCrossRefGoogle Scholar
  20. Noble DWA, Carazo P, Whiting MJ (2012) Learning outdoors: male lizards show flexible spatial learning under semi-natural conditions. Biol Lett 8:946–948Google Scholar
  21. Paulissen MA (2008) Spatial learning in the little brown skink, Scincella lateralis: the importance of experience. Anim Behav 76:135–141CrossRefGoogle Scholar
  22. Rice D, Barone S Jr (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Persp 108(Suppl 3):511–533Google Scholar
  23. Shettleworth SJ (2009) Cognition, evolution, and behavior. Oxford University Press, New YorkGoogle Scholar
  24. Shine R (2004a) Incubation regimes of cold-climate reptiles: the thermal consequences of nest-site choice, viviparity and maternal basking. Biol J Linn Soc 83:145–155Google Scholar
  25. Shine R (2004b) Does viviparity evolve in cold climate reptiles because pregnant females maintain stable (not high) body temperatures? Evolution 58:1809–1818Google Scholar
  26. Shine R, Elphick MJ, Harlow PS (1997) The influence of natural incubation environments on the phenotypic traits of hatchling lizards. Ecology 78:2559–2568CrossRefGoogle Scholar
  27. Sih A, Moore RD (1993) Delayed hatching of salamander eggs in response to enhanced larval predation risk. Am Nat 142:947–960PubMedCrossRefGoogle Scholar
  28. Tomporowski P, Davis C, Miller P, Naglieri J (2008) Exercise and children’s intelligence, cognition, and academic achievement. Educ Psychol Rev 20:111–131PubMedCentralPubMedCrossRefGoogle Scholar
  29. Warkentin KM, Caldwell MS (2009) Assessing risk: embryos, information, and escape hatching. In: Dukas R, Ratcliffe J (eds) Cognitive ecology II: the evolutionary ecology of learning, memory, and information use. University of Chicago Press, Chicago, pp 177–200CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Benjamin F. Clark
    • 1
  • Joshua J. Amiel
    • 2
  • Richard Shine
    • 2
  • Daniel W. A. Noble
    • 1
  • Martin J. Whiting
    • 1
    Email author
  1. 1.Department of Biological SciencesMacquarie UniversitySydneyAustralia
  2. 2.School of Biological SciencesUniversity of SydneySydneyAustralia

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