Oecologia

pp 1–10 | Cite as

Mate familiarity and social learning in a monogamous lizard

  • Kirke L. Munch
  • Daniel W. A. Noble
  • Erik Wapstra
  • Geoffrey M. While
Highlighted Student Research

Abstract

Social learning is thought to be advantageous as it allows an animal to gather information quickly without engaging in costly trial-and-error learning. However, animals should be selective about when and whom they learn from. Familiarity is predicted to positively influence an animal’s reliance on social learning; yet, few studies have empirically tested this theory. We used a lizard (Liopholis whitii) that forms long-term monogamous pair bonds to examine the effects of partner familiarity on social learning in two novel foraging tasks, an association and a reversal task. We allowed female lizards to observe trained conspecifics that were either familiar (social mate) or unfamiliar execute these tasks and compared these two groups with control females that did not receive social information. Lizards preferentially relied on trial-and-error learning in the association task. In the reversal task, lizards that were demonstrated by familiar partners learnt in fewer trials compared to control lizards and made more correct choices. Our results provide some evidence for context-dependent learning with lizards differentiating between when they utilize social learning, and, to a limited degree, whom they learnt from. Understanding the role of the social context in which learning occurs provides important insights into the benefits of social learning and sociality more generally.

Keywords

Cognition Social learning Familiarity Reptiles Egernia 

Notes

Acknowledgements

We would like to thank two anonymous reviewers and the handling editor for their constructive feedback on previous versions of the manuscript. We are grateful to Giles Barrington for scoring a subset of our video footage, and we would like to thank the numerous members of the Behavioural and Evolutionary Ecology group that assisted us with lizard collection, husbandry and experimental setup.

Author contribution statement

KLM, DWAN, EW and GMW conceived and designed the study. KLM carried out the field and laboratory work. KLM analysed the data with assistance from DWAN and GMW. KLM wrote the paper with assistance from all authors.

Funding

This research was supported by the Australian Research Council (DP150102900 to GMW) and a Holsworth Wildlife Endowment Grant (to KLM). KLM was supported by a University of Tasmania PhD scholarship. GMW (DE150100336), EW (FT110100597), and DWAN (DE150101774) were supported by the Australian Research Council.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional and national guidelines for the care and use of animals were followed. All of the work described here was conducted with the approval of the University of Tasmania’s Animal Ethics Committee (A14536).

Supplementary material

442_2018_4153_MOESM1_ESM.docx (77 kb)
Supplementary material 1 (DOCX 77 kb)
442_2018_4153_MOESM2_ESM.csv (259 kb)
Supplementary material 2 (CSV 259 kb)
442_2018_4153_MOESM3_ESM.csv (374 kb)
Supplementary material 3 (CSV 373 kb)

References

  1. Amiel JJ, Lindstrom J, Shine R (2014) Egg incubation effects generate positive correlations between size, speed and learning ability in young lizards. Anim Cognit 17:337–347.  https://doi.org/10.1007/s10071-013-0665-4 CrossRefGoogle Scholar
  2. Aplin LM, Farine DR, Morand-Ferron J, Cockburn A, Thornton A, Sheldon BC (2015) Experimentally induced innovations lead to persistent culture via conformity in wild birds. Nature 518:538–541.  https://doi.org/10.1038/nature13998 CrossRefPubMedGoogle Scholar
  3. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48.  https://doi.org/10.18637/jss.v067.i01 CrossRefGoogle Scholar
  4. Beauchamp G, Kacelnik A (1991) Effects of the knowledge of partners on learning rates in zebra finches Taeniopygia guttata. Anim Behav 41:247–253.  https://doi.org/10.1016/S0003-3472(05)80476-2 CrossRefGoogle Scholar
  5. Benskin CMH, Mann NI, Lachlan RF, Slater PJB (2002) Social learning directs feeding preferences in the zebra finch, Taeniopygia guttata. Anim Behav 64:823–828.  https://doi.org/10.1006/anbe.2002.2005 CrossRefGoogle Scholar
  6. Black JM (1996) Introduction: pair bonds and partnerships. In: Black JM (ed) Partnerships in birds. The study of monogamy. Oxford University Press, Oxford, pp 3–20Google Scholar
  7. Boyd R, Richerson PJ (1988) Culture and the evolutionary process. University of Chicago Press, ChicagoGoogle Scholar
  8. Brown C, Laland KN (2003) Social learning in fishes: a review. Fish Fish 4:280–288.  https://doi.org/10.1046/j.1467-2979.2003.00122.x CrossRefGoogle Scholar
  9. Bull MC (2000) Monogamy in lizards. Behav Process 51:7–20.  https://doi.org/10.1016/S0376-6357(00)00115-7 CrossRefGoogle Scholar
  10. Carazo P, Noble DWA, Chandrasoma D, Whiting MJ (2014) Sex and boldness explain individual differences in spatial learning in a lizard. Proc R Soc B 281:20133275.  https://doi.org/10.1098/rspb.2013.3275 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 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.  https://doi.org/10.1655/0733-1347(2003)017[0145:ELABIT]2.0.CO;2 CrossRefGoogle Scholar
  12. Chapple DG, Keogh JS (2005) Complex mating system and dispersal patterns in a social lizard, Egernia whitii. Mol Ecol 14:1215–1227.  https://doi.org/10.1111/j.1365-294X.2005.02486.x CrossRefPubMedGoogle Scholar
  13. 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.  https://doi.org/10.1007/s00265-013-1639-x CrossRefGoogle Scholar
  14. Cohen J (1988) Statistical power analysis for the behavioral sciences. Lawrence Earlbaum Associates, HillsideGoogle Scholar
  15. Coussi-Korbel S, Fragaszy DM (1995) On the relation between social dynamics and social learning. Anim Behav 50:1441–1453.  https://doi.org/10.1016/0003-3472(95)80001-8 CrossRefGoogle Scholar
  16. Day RL, Coe RL, Kendal JR, Laland KN (2003) Neophilia, innovation and social learning: a study of intergeneric differences in callitrichid monkeys. Anim Behav 65:559–571.  https://doi.org/10.1006/anbe.2003.2074 CrossRefGoogle Scholar
  17. Dayananda B, Webb JK (2017) Incubation under climate warming affects learning ability and survival in hatchling lizards. Biol Lett.  https://doi.org/10.1098/rsbl.2017.0002 Google Scholar
  18. Duboscq J, Romano V, MacIntosh A, Sueur C (2016) Social information transmission in animals: lessons from studies of diffusion. Front Psychol.  https://doi.org/10.3389/fpsyg.2016.01147 PubMedPubMedCentralGoogle Scholar
  19. Duffy GA, Pike TW, Laland KN (2009) Size-dependent directed social learning in nine-spined sticklebacks. Anim Behav 78:371–375.  https://doi.org/10.1016/j.anbehav.2009.05.015 CrossRefGoogle Scholar
  20. Galef BG Jr, Giraldeau L (2001) Social influences on foraging in vertebrates: causal mechanisms and adaptive functions. Anim Behav 61:3–15.  https://doi.org/10.1006/anbe.2000.1557 CrossRefPubMedGoogle Scholar
  21. Galef BG Jr, Laland K (2005) Social learning in animals: empirical studies and theoretical models. Bioscience 55:489–499.  https://doi.org/10.1641/0006-3568(2005)055[0489:SLIAES]2.0.CO;2 CrossRefGoogle Scholar
  22. Galef JBG, White DJ (1998) Mate-choice copying in Japanese quail, Coturnix japonica. Anim Behav 55:545–552.  https://doi.org/10.1006/anbe.1997.0616 CrossRefGoogle Scholar
  23. Griffiths SW (2003) Learned recognition of conspecifics by fishes. Fish Fish 4:256–268.  https://doi.org/10.1046/j.1467-2979.2003.00129.x CrossRefGoogle Scholar
  24. Guillette LM, Scott ACY, Healy SD (2016) Social learning in nest-building birds: a role for familiarity. Proc R Soc B 283:20152685.  https://doi.org/10.1098/rspb.2015.2685 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Halliwell B, Uller T, Wapstra E, While GM (2017) Resource distribution mediates social and mating behavior in a family living lizard. Behav Ecol 28:145–153.  https://doi.org/10.1093/beheco/arw134 CrossRefGoogle Scholar
  26. Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156.  https://doi.org/10.2307/177062 CrossRefGoogle Scholar
  27. Heyes CM (1994) Social learning in animals: categories and mechanisms. Biol Rev Camb Philos Soc 69:207–231.  https://doi.org/10.1111/j.1469-185X.1994.tb01506.x CrossRefPubMedGoogle Scholar
  28. Heyes CM (2016) Who knows? Metacognitive social learning strategies. Trends Cogn Sci 20:204–213.  https://doi.org/10.1016/j.tics.2015.12.007 CrossRefPubMedGoogle Scholar
  29. Heyes C, Pearce JM (2015) Not-so-social learning strategies. Proc Biol Sci.  https://doi.org/10.1098/rspb.2014.1709 PubMedPubMedCentralGoogle Scholar
  30. Hoppitt W, Laland K (2013) Social learning: on introduction to mechanisms, methods, and models. Princeton University Press, PrincetonCrossRefGoogle Scholar
  31. Kar F, Whiting MJ, Noble DWA (2017) Dominance and social information use in a lizard. Anim Cogn 20:805–812.  https://doi.org/10.1007/s10071-017-1101-y CrossRefPubMedGoogle Scholar
  32. Kaufman AB, Rosenthal R (2009) Can you believe my eyes? The importance of interobserver reliability statistics in observation of animal behaviour. Anim Behav 78:1487–1491.  https://doi.org/10.1016/j.anbehav.2009.09.014 CrossRefGoogle Scholar
  33. Kavaliers M, Colwell DD, Choleris E (2005) Kinship, familiarity and social status modulate social learning about “micropredators” (biting flies) in deer mice. Behav Ecol Sociobiol 58:60–71.  https://doi.org/10.1007/s00265-004-0896-0 CrossRefGoogle Scholar
  34. Kawai M (1965) Newly-acquired pre-cultural behavior of the natural troop of Japanese monkeys on Koshima islet. Primates 6:1–30.  https://doi.org/10.1007/bf01794457 CrossRefGoogle Scholar
  35. Kendal RL, Coolen I, van Bergen Y, Laland KN (2005) Trade-offs in the adaptive use of social and asocial learning. Adv Study Behav 35:333–379.  https://doi.org/10.1016/s0065-3454(05)35008-x CrossRefGoogle Scholar
  36. Lachlan RF, Crooks L, Laland KN (1998) Who follows whom? Shoaling preferences and social learning of foraging information in guppies Anim Behav 56:181–190.  https://doi.org/10.1006/anbe.1998.0760 PubMedGoogle Scholar
  37. LaDage LD, Riggs BJ, Sinervo B, Pravosudiv VV (2009) Dorsal cortex volume in male side-blotched lizards (Uta stansburiana) is associated with different space use strategies. Anim Behav 78:91–96.  https://doi.org/10.1016/j.anbehav.2009.03.020 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Laland KN (2004) Social learning strategies. Learn Behav 32:4–14.  https://doi.org/10.3758/BF03196002 CrossRefPubMedGoogle Scholar
  39. Leris I, Reader SM (2016) Age and early social environment influence guppy social learning propensities. Anim Behav 120:11–19.  https://doi.org/10.1016/j.anbehav.2016.07.012 CrossRefGoogle Scholar
  40. Leu ST, Burzacott D, Whiting MJ, Bull CM (2015) Mate familiarity affects pairing behaviour in a long-term monogamous lizard: evidence from detailed bio-bogging and a 31-year field study. Ethology 121:760–768.  https://doi.org/10.1111/eth.12390 CrossRefGoogle Scholar
  41. Lonsdorf EV, Bonnie KE (2010) Opportunities and constraints when studying social learning: developmental approaches and social factors. Learn Behav 38:195–205.  https://doi.org/10.3758/lb.38.3.195 CrossRefPubMedGoogle Scholar
  42. Munch KL, Noble DWA, Botterill-James T, Koolhof IS, Halliwell B, Wapstra E, While GM (2018) Maternal effects on decision-making in a viviparous lizard. Biol Lett.  https://doi.org/10.1098/rsbl.2017.0556 PubMedGoogle Scholar
  43. Nicol CJ, Pope SJ (1994) Social learning in small flocks of laying hens. Anim Behav 47:1289–1296.  https://doi.org/10.1016/j.anbehav.2007.06.006 CrossRefGoogle Scholar
  44. Nicol CJ, Pope SJ (1999) The effects of demonstrator social status and prior foraging success on social learning in laying hens. Anim Behav 57:163–171.  https://doi.org/10.1006/anbe.1998.0920 CrossRefPubMedGoogle Scholar
  45. Noble DWA, Carazo P, Whiting MJ (2012) Learning outdoors: male lizards show flexible spatial learning under semi-natural conditions. Biol Lett 8:946–948.  https://doi.org/10.1098/rsbl.2012.0813 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Noble DW, Byrne RW, Whiting MJ (2014) Age-dependent social learning in a lizard. Biol Lett 10:20140430.  https://doi.org/10.1098/rsbl.2014.0430 CrossRefPubMedPubMedCentralGoogle Scholar
  47. R Core Team (2016) R: A language and environment for statistical computing. Vienna, Austria. R Foundation for Statistical Computing. See http://R-project.org
  48. Revelle W (2017) “psych”: procedures for personality and psychological research. See https://CRAN.R-project.org/package=psych, version 1.7.8
  49. Riley JL, Noble DWA, Byrne RW, Whiting Mj (2017) Does social environment influence learning ability in a family-living lizard? Anim Cogn 20:449–458.  https://doi.org/10.1007/s10071-016-1068-0 CrossRefPubMedGoogle Scholar
  50. Sanchez-Macouzet O, Rodriguez C, Drummond H (2014) Better stay together: pair bond duration increases individual fitness independent of age-related variation. Proc R Soc B 281:7.  https://doi.org/10.1098/rspb.2013.2843 CrossRefGoogle Scholar
  51. Scheid C, Range F, Bugnyar T (2007) When, what, and whom to watch? Quantifying attention in ravens (Corvus corax) and jackdaws (Corvus monedula). J Comp Psychol 121:380–386.  https://doi.org/10.1037/0735-7036.121.4.380 CrossRefPubMedGoogle Scholar
  52. Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods Ecol Evol 1:103–113.  https://doi.org/10.1111/j.2041-210X.2010.00012.x CrossRefGoogle Scholar
  53. Schwab C, Bugnyar T, Kotrschal K (2008) Preferential learning from non-affiliated individuals in jackdaws (Corvus monedula). Behav Process 79:148–155.  https://doi.org/10.1016/j.beproc.2008.07.002 CrossRefGoogle Scholar
  54. Shettleworth SJ (2010) Cognition, evolution, and behavior, 2nd edn. Oxford University Press, New YorkGoogle Scholar
  55. Swaney W, Kendal J, Capon H, Brown C, Laland KN (2001) Familiarity facilitates social learning of foraging behaviour in the guppy. Anim Behav 62:591–598.  https://doi.org/10.1006/anbe.2001.1788 CrossRefGoogle Scholar
  56. Templeton JJ (1998) Learning from others’ mistakes: a paradox revisited. Anim Behav 55:79–85.  https://doi.org/10.1006/anbe.1997.0587 CrossRefPubMedGoogle Scholar
  57. Trompf L, Brown C (2014) Personality affects learning and trade-offs between private and social information in guppies, Poecilia reticulata. Anim Behav 88:99–106.  https://doi.org/10.1016/j.anbehav.2013.11.022 CrossRefGoogle Scholar
  58. van de Waal E, Renevey N, Favre CM, Bshary R (2010) Selective attention to philopatric models causes directed social learning in wild vervet monkeys. Proc R Soc B 277:2105–2111.  https://doi.org/10.1098/rspb.2009.2260 CrossRefPubMedPubMedCentralGoogle Scholar
  59. While GM, Uller T, Wapstra E (2009a) Family conflict and the evolution of sociality in reptiles. Behav Ecol 20:245–250.  https://doi.org/10.1093/beheco/arp015 CrossRefGoogle Scholar
  60. While GM, Uller T, Wapstra E (2009b) Within-population variation in social strategies characterize the social and mating system of an Australian lizard, Egernia whitii. Austral Ecol 34:938–949.  https://doi.org/10.1111/j.1442-9993.2009.02002.x CrossRefGoogle Scholar
  61. While GM, Chapple DG, Gardner MG, Uller T, Whiting MJ (2015) Egernia lizards. Curr Biol 25:R593–R595.  https://doi.org/10.1016/j.cub.2015.02.070 CrossRefPubMedGoogle Scholar
  62. Wilkinson A, Kuenstner K, Mueller J, Huber L (2010a) Social learning in a non-social reptile (Geochelone carbonaria). Biol Lett 6:614–616.  https://doi.org/10.1098/rsbl.2010.0092 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Wilkinson A, Specht HL, Huber L (2010b) Pigeons can discriminate group mates from strangers using the concept of familiarity. Anim Behav 80:109–115.  https://doi.org/10.1016/j.anbehav.2010.04.006 CrossRefGoogle Scholar
  64. Wilson S, Swan G (2003) A complete guide to reptiles of Australia. Reed New Holland, SydneyGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of TasmaniaHobartAustralia
  2. 2.School of Biological, Earth, and Environmental SciencesUniversity of New South WalesKensingtonAustralia

Personalised recommendations