Animal Cognition

, Volume 20, Issue 3, pp 449–458 | Cite as

Does social environment influence learning ability in a family-living lizard?

  • Julia L. RileyEmail author
  • Daniel W. A. Noble
  • Richard W. Byrne
  • Martin J. Whiting
Original Paper


Early developmental environment can have profound effects on individual physiology, behaviour, and learning. In birds and mammals, social isolation during development is known to negatively affect learning ability; yet in other taxa, like reptiles, the effect of social isolation during development on learning ability is unknown. We investigated how social environment affects learning ability in the family-living tree skink (Egernia striolata). We hypothesized that early social environment shapes cognitive development in skinks and predicted that skinks raised in social isolation would have reduced learning ability compared to skinks raised socially. Offspring were separated at birth into two rearing treatments: (1) raised alone or (2) in a pair. After 1 year, we quantified spatial learning ability of skinks in these rearing treatments (N = 14 solitary, 14 social). We found no effect of rearing treatment on learning ability. The number of skinks to successfully learn the task, the number of trials taken to learn the task, the latency to perform the task, and the number of errors in each trial did not differ between isolated and socially reared skinks. Our results were unexpected, yet the facultative nature of this species’ social system may result in a reduced effect of social isolation on behaviour when compared to species with obligate sociality. Overall, our findings do not provide evidence that social environment affects development of spatial learning ability in this family-living lizard.


Squamate Sociality Cognition Ontogeny Facultative sociality 



We thank G. While and M. Favre for their assistance in the field and laboratory, as well as J. Baxter-Gilbert and F. Kar for their artistic and statistical advice.


Financial support for this research was provided by the Australian Research Council (DP130102998, awarded to MJW and RWB), Natural Sciences and Engineering Research Council of Canada (scholarship to JLR), the Australasian Society for the Study of Animal Behaviour, the Australian Museum, and Macquarie University. DWAN was supported by an ARC Discovery Early Career Research Award (DE150101774) and UNSW Vice Chancellors Fellowship.

Compliance with ethical standards

Conflict of interest

All the authors declare they have no conflict of interest.

Ethical approval

We followed guidelines for the care and use of animals as laid out by the Association for the Study of Animal Behaviour. Experimental protocols were approved by the Macquarie University Animal Ethics Committee (ARA # 2013/039). Collection of skinks was approved by the New South Wales National Parks and Wildlife Service, Office of Environment and Heritage (License # SL101264). Female skinks were captured either by hand, noosing or Eliot trap and were placed in cloth bags until they could be transported by vehicle to Macquarie University from Albury, New South Wales, in an insulated box. We observed no injuries resulting from our cognition experiment.

Supplementary material

10071_2016_1068_MOESM1_ESM.docx (148 kb)
Supplementary material 1 (DOCX 148 kb)

Supplementary material 2 (MOV 73617 kb)


  1. Ballen C, Shine R, Olsson M (2014) Effects of early social isolation on the behaviour and performance of juvenile lizards, Chamaeleo calyptratus. Anim Behav 88:1–6. doi: 10.1016/j.anbehav.2013.11.010 CrossRefGoogle Scholar
  2. Bonnett MP (1999) The ecology, behaviour and genetic relationships of a population of Egernia striolata. Unpublished Honours thesis, Flinders University of South Australia, Adelaide, AustraliaGoogle Scholar
  3. Buchanan KL, Grindstaff JL, Pravosudov VV (2013) Condition dependence, developmental plasticity, and cognition: implications for ecology and evolution. Trends Ecol Evol 28:290–296. doi: 10.1016/j.tree.2013.02.004 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Burkart JM, van Schaik CP (2009) Cognitive consequences of cooperative breeding in primates? Anim Cogn 13:1–19. doi: 10.1007/s10071-009-0263-7 CrossRefPubMedGoogle Scholar
  5. Bustard HR (1970) A population study of the scincid lizard Egernia striolata in northern New South Wales. Proc K Ned Akad Wet C 73:202Google Scholar
  6. Cacioppo JT, Hawkley LC (2009) Perceived social isolation and cognition. Trends Cogn Sci 13:447–454. doi: 10.1016/j.tics.2009.06.005 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Carazo P, Noble DWA, Chandrasoma D, Whiting MJ (2014) Sex and boldness explain individual differences in spatial learning in a lizard. Proc Biol Sci 281:20133275. doi: 10.1098/rspb.2013.3275 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cauchard L, Boogert NJ, Lefebvre L, Dubois F, Doligez B (2013) Problem-solving performance is correlated with reproductive success in a wild bird population. Anim Behav 85:19–26. doi: 10.1016/j.anbehav.2012.10.005 CrossRefGoogle Scholar
  9. Chapple DG (2003) Ecology, life-history, and behavior in the Australian scincid genus Egernia, with comments on the evolution of complex sociality in lizards. Herpetol Monogr 17:145–180. doi:10.1655/0733-1347(2003)017[0145:elabit];2CrossRefGoogle Scholar
  10. Clark BF, Amiel JJ, Shine R, Noble DWA, Whiting MJ (2013) Colour discrimination and associative learning in hatchling lizards incubated at ‘hot’ and ‘cold’ temperatures. Behav Ecol Sociobiol 68:239–247. doi: 10.1007/s00265-013-1639-x CrossRefGoogle Scholar
  11. Cogger HG (2014) Reptiles and amphibians of Australia, 7th edn. CSIRO Publishing, ClaytonGoogle Scholar
  12. Cunningham RB, Lindenmayer DB, Crane M, Michael D, MacGregor C (2007) Reptile and arboreal marsupial response to replanted vegetation in agricultural landscapes. Ecol Appl 17:609–619. doi: 10.1890/05-1892 CrossRefPubMedGoogle Scholar
  13. De Vosjoli P, Ferguson G (1995) Care and breeding of Panther, Jackson’s, Veiled, and Parson’s chameleons. i5 Publishing, Los AngelesGoogle Scholar
  14. Dobson AJ, Barnett A (2008) An introduction to generalized linear models. CRC Press, Boca Raton, pp 45–66, 229–256Google Scholar
  15. Doody JS, Burghardt GM, Dinets V (2012) Breaking the social-non-social dichotomy: a role for reptiles in vertebrate social behavior research? Ethology 119:95–103. doi: 10.1111/eth.12047 CrossRefGoogle Scholar
  16. Duckett PE, Morgan MH, Stow AJ (2012) Tree-dwelling populations of the skink Egernia striolata aggregate in groups of close kin. Copeia 2012:130–134. doi: 10.1643/ce-10-183 CrossRefGoogle Scholar
  17. Dukas R (2009) Learning: mechanisms, ecology and evolution. In: Dukas R, Ratcliffe JM (eds) Cognitive ecology II. The University of Chicago Press, Chicago, pp 7–26CrossRefGoogle Scholar
  18. Dukas R, Bernays EA (2000) Learning improves growth rate in grasshoppers. Proc Natl Acad Sci USA 97:2637–2640. doi: 10.1073/pnas.050461497 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Ehmann H (1992) Encyclopedia of Australian animals: reptiles. Angus and Robertson, SydneyGoogle Scholar
  20. Einon D (1980) Spatial memory and response strategies in rats: age, sex and rearing differences in performance. Q J Exp Psychol 32:473–489. doi: 10.1080/14640748008401840 CrossRefPubMedGoogle Scholar
  21. Fooden J (2000) Systematic review of the rhesus macaque, Macaca mulatta (Zimmermann, 1780). Field Zool 96:1–180. doi: 10.5962/bhl.title.7192 Google Scholar
  22. Frisone DF, Frye CA, Zimmerberg B (2002) Social isolation stress during the third week of life has age-dependent effects on spatial learning in rats. Behav Brain Res 128:153–160. doi: 10.1016/S0166-4328(01)00315-1 CrossRefPubMedGoogle Scholar
  23. Gardner MG, Pearson SK, Johnston GR, Schwarz MP (2015) Group living in squamate reptiles: a review of evidence for stable aggregations. Biol Rev Camb Philos Soc. doi: 10.1111/brv.12201 PubMedGoogle Scholar
  24. Gelman A, Carlin JB, Stern HS, Rubin DB (2014) Bayesian data analysis, vol 3. Chapman and Hall/CRC Press, Boca RatonGoogle Scholar
  25. Goerlich VC, Nätt D, Elfwing M, Macdonald B, Jensen P (2012) Transgenerational effects of early experience on behavioral, hormonal and gene expression responses to acute stress in the precocial chicken. Horm Behav 61:711–718. doi: 10.1016/j.yhbeh.2012.03.006 CrossRefPubMedGoogle Scholar
  26. Greenough WT, Madden TC, Fleischmann TB (1972) Effects of isolation, daily handling, and enriched rearing on maze learning. Psychon Sci 27:279–280. doi: 10.3758/bf03328961 CrossRefGoogle Scholar
  27. Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22. doi: 10.18637/jss.v033.i02 CrossRefGoogle Scholar
  28. Harlow HF, Dodsworth RO, Harlow MK (1965) Total social isolation in monkeys. Proc Natl Acad Sci USA 54:90–97. doi: 10.1073/pnas.54.1.90 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Holson RR (1986) Feeding neophobia: a possible explanation for the differential maze performance of rats reared in enriched or isolated environments. Physiol Behav 38:191–201. doi: 10.1016/0031-9384(86)90154-X CrossRefPubMedGoogle Scholar
  30. Isden J, Panavi C, Dingle C, Madden J (2013) Performance in cognitive and problem-solving tasks in male spotted bowerbirds does not correlate with mating success. Anim Behav 86:829–838. doi: 10.1016/j.anbehav.2013.07.024 CrossRefGoogle Scholar
  31. Juraska JM, Henderson C, Müller J (1984) Differential rearing experience, gender, and radial maze performance. Dev Psychobiol 17:209–215. doi: 10.1002/dev.420170302 CrossRefPubMedGoogle Scholar
  32. Keagy J, Savard JF, Borgia G (2009) Male satin bowerbird problem-solving ability predicts mating success. Anim Behav 78:809–817. doi: 10.1016/j.anbehav.2009.07.011 CrossRefGoogle Scholar
  33. Kruschke J (2014) Doing Bayesian data analysis: a tutorial with R, JAGS and Stan. Academic Press, CambridgeGoogle Scholar
  34. Langkilde T, O’Connor D, Shine R (2007) Benefits of parental care: do juvenile lizards obtain better-quality habitat by remaining with their parents? Austral Ecol 32:950–954. doi: 10.1111/j.1442-9993.2007.01783.x CrossRefGoogle Scholar
  35. Lanham EJ, Bull CM (2000) Maternal care and infanticide in the Australian skink, Egernia stokesii. Herpetol Rev 31:151–152. doi: 10.1016/j.anbehav.2004.02.014 Google Scholar
  36. Masson ME (2011) A tutorial on a practical Bayesian alternative to null-hypothesis significance testing. Behav Res Methods 43:679–690. doi: 10.3758/s13428-010-0049-5 CrossRefPubMedGoogle Scholar
  37. Melnick DJ, Pearl MC, Richard AF (1984) Male migration and inbreeding avoidance in wild rhesus monkeys. Am J Primatol 7:229–243. doi: 10.1002/ajp.1350070303 CrossRefGoogle Scholar
  38. Michael DR, Cunningham RB (2010) The social elite: habitat heterogeneity, complexity and quality in granite inselbergs influence patterns of aggregation in Egernia striolata (Lygosominae: Scincidae). Austral Ecol 35:862–870. doi: 10.1111/j.1442-9993.2009.02092.x CrossRefGoogle Scholar
  39. Morgan MJ, Einon DF, Nicholas D (1975) The effects of isolation rearing on behavioural inhibition in the rat. Q J Exp Psychol 27:615–634. doi: 10.1080/14640747508400524 CrossRefGoogle Scholar
  40. Naguib M, Flörcke C, van Oers K (2011) Effects of social conditions during early development on stress response and personality traits in great tits (Parus major). Dev Psychobiol 53:592–600. doi: 10.1002/dev.20533 CrossRefPubMedGoogle Scholar
  41. Noble DWA, Carazo P, Whiting MJ (2012) Learning outdoors: male lizards show flexible spatial learning under semi-natural conditions. Biol Lett 8:946–948. doi: 10.1098/rsbl.2012.0813 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Noble DWA, Byrne RW, Whiting MJ (2014) Age-dependent social learning in a lizard. Biol Lett 10:20140430. doi: 10.1098/rsbl.2014.0430 CrossRefPubMedPubMedCentralGoogle Scholar
  43. O’Connor DE, Shine R (2004) Parental care protects against infanticide in the lizard Egernia saxatilis (Scincidae). Anim Behav 68:1361–1369. doi: 10.1016/j.anbehav.2004.02.014 CrossRefGoogle Scholar
  44. Plummer M, Best N, Cowles K, Vines K (2015) Coda: output analysis and diagnostics for MCMC. R package version 0.13-3.
  45. Post MJ (2000) The captive husbandry and reproduction of the Hosmer’s Skink Egernia hosmeri. Herpetofauna 30:2–6Google Scholar
  46. Roth TC, LaDage LD, Pravosudov VV (2010) Learning capabilities enhanced in harsh environments: a common garden approach. Proc R Soc B Biol 277:3187–3193. doi: 10.1098/rspb.2010.0630 CrossRefGoogle Scholar
  47. R Core Team (2016) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
  48. Shettleworth SJ (2010) Cognition, evolution, and behavior, 2nd edn. Oxford University Press, New YorkGoogle Scholar
  49. Sih A, Del Giudice M (2012) Linking behavioural syndromes and cognition: a behavioural ecology perspective. Philos Trans R Soc Lond B 367:2762–2772. doi: 10.1098/rstb.2012.0216 CrossRefGoogle Scholar
  50. Sih A, Ferrari MCO, Harris DJ (2011) Evolution and behavioural responses to human-induced rapid environmental change. Evol Appl 4:367–387. doi: 10.1111/j.1752-4571.2010.00166.x CrossRefPubMedPubMedCentralGoogle Scholar
  51. Sinn DL, While GM, Wapstra E (2008) Maternal care in a social lizard: links between female aggression and offspring fitness. Anim Behav 76:1249–1257. doi: 10.1016/j.anbehav.2008.06.009 CrossRefGoogle Scholar
  52. Sol D, Lapiedra O, González-Lagos C (2013) Behavioural adjustments for a life in the city. Anim Behav 85:1101–1112. doi: 10.1016/j.anbehav.2013.01.023 CrossRefGoogle Scholar
  53. Stamps JA, Groothuis TGG (2010) Developmental perspectives on personality: implications for ecological and evolutionary studies of individual differences. Philos Trans R Soc Lond B 365:4029–4041. doi: 10.1098/rstb.2010.0218 CrossRefGoogle Scholar
  54. Swanson S (1976) Lizards of Australia. Angus and Robertson, Sydney, p 43Google Scholar
  55. Thorton A, Isden J, Madden JR (2014) Toward wild psychometrics: linking individual cognitive differences to fitness. Behav Ecol 25:1299–1301. doi: 10.1093/beheco/aru095 CrossRefGoogle Scholar
  56. While GM, Chapple DG, Gardner MG et al (2015) Egernia lizards. Curr Biol 25:R593–R595. doi: 10.1016/j.cub.2015.02.070 CrossRefPubMedGoogle Scholar
  57. Wongwitdecha N, Marsden CA (1996) Effects of social isolation rearing on learning in the Morris water maze. Brain Res 715:119–124. doi: 10.1016/0006-8993(95)01578-7 CrossRefPubMedGoogle Scholar
  58. Zuberbühler K, Byrne RW (2006) Social cognition. Curr Biol 16:R786–R790. doi: 10.1016/j.cub.2006.08.046 CrossRefPubMedGoogle Scholar
  59. Zurr AF, Hilbe JM, Ieno EN (2013) A beginner’s guide to GLM and GLMM with R: a frequentist and Bayesian perspective for ecologists. Highland Statistics Ltd, NewburghGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of Biological SciencesMacquarie UniversitySydneyAustralia
  2. 2.School of Biological, Earth, and Environmental SciencesUniversity of New South WalesKensingtonAustralia
  3. 3.School of Psychology and NeuroscienceUniversity of St. AndrewsSt. AndrewsUK

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