Why blue tongue? A potential UV-based deimatic display in a lizard

  • Arnaud Badiane
  • Pau Carazo
  • Samantha J. Price-Rees
  • Manuel Ferrando-Bernal
  • Martin J. WhitingEmail author
Original Article


Deimatic displays are a type of anti-predator behaviour that startles the predator. They have received much recent theoretical attention, enabling the empirical study of this phenomenon within a predictive framework. It has long been known that bluetongue skinks (Tiliqua spp.), when approached by predators, open their mouth widely and expose a conspicuously coloured tongue. Here, we test whether such ‘full-tongue’ displays are triggered by an imminent predatory attack in the Northern Bluetongue skink Tiliqua scincoides intermedia and examine whether this display behaviour is consistent with the predictions from deimatic display theory. First, we demonstrate that luminance at the rear of the tongue, which is only exposed during full-tongue displays, is almost twice as high for lizard and bird receivers compared to the tip of the tongue, and that tongue colouration is generally more conspicuous to a bird than a lizard visual system. Second, staged predatory encounters using model predators reveal that lizards primarily exhibit full-tongue displays in the final stages of a predatory attack. Lizards performed full-tongue displays congruent with the predictions associated with deimatic displays, i.e. rapid exposure of conspicuous elements from a previously inconspicuous state concurrently with aggressive defensive behaviour, most frequently during the final stages of a predatory encounter. Surprisingly, we also found that lizards vary the area of the tongue exposed during chemoexploratory tongue-flicks depending on whether a predator is present or absent.

Significance statement

Bluetongue skinks have long been known to expose their large blue tongue in response to predatory threats. However, this behaviour has never been investigated empirically. Here, we use Northern Bluetongue skinks (Tiliqua scincoides intermedia) to test whether this behaviour is consistent with predictions associated with deimatic displays. We show that the rear of their tongue is UV-blue and more conspicuous to predators compared to the tip and that this ‘full-tongue display’ is only triggered in the final stages of a predatory attack.


Deimatic displays Anti-predator behaviour Reptile Coloration 



We are grateful to Grant Napier for his invaluable field assistance, Sarah Pryke for loaning us a reflectance spectrophotometer, and Bill Stewart and Corrin Everitt for making their property available for our study. We also thank two anonymous reviewers for improving this manuscript.

Authors’ contributions

MJW and PC conceived the study. SJPR, PC, and MJW conducted the experiments and collected the morphological and colour measurements. AB scored the behaviours. MFB took the tongue measurements. AB and PC carried out the statistical analyses. AB, PC, and MJW drafted the manuscript, and all authors provided feedback.


This work was supported by funding to MJW from Macquarie University. AB was funded by an iMQRES doctoral scholarship awarded by Macquarie University (2014166), and PC was funded by an Endeavour fellowship.

Compliance with ethical standards

Ethical approval

For the handling of animals, we followed the ABS (Animal Behavior Society)/ASAB (Association for the Study of Animal Behaviour) ‘Guidelines for the treatment of animals in behavioural research and teaching’. Our research protocols were approved by the Macquarie University Animal Ethics Committee and University of Sydney Animal Care and Ethics Committee, Parks and Wildlife Commission of the Northern Territory, and the Western Australian Department of Environment and Conservation.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abramjan A, Bauerová A, Somerová B, Frynta D (2015) Why is the tongue of blue-tongued skinks blue? Reflectance of lingual surface and its consequences for visual perception by conspecifics and predators. Naturwissenschaften 102:1–12CrossRefGoogle Scholar
  2. Bateman AW, Vos M, Anholt BR (2014) When to defend: antipredator defenses and the predation sequence. Am Nat 183:847–855CrossRefPubMedGoogle Scholar
  3. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version, 1(7).
  4. Belcher CA (1995) Diet of the tiger quoll (Dasyurus maculatus). Wildl Res 22:341–357CrossRefGoogle Scholar
  5. Blumstein DT, Evans CS, Daniel JC (2006) JWatcher 1.0.
  6. Bradbury JW, Vehrencamp SL (2011) Principles of animal communication, 2nd edn. Sinauer Associates, SunderlandGoogle Scholar
  7. Carazo P, Font E, Desfilis E (2007) Chemosensory assessment of rival competitive ability and scent-mark function in a lizard, Podarcis hispanica. Anim Behav 74:895–902CrossRefGoogle Scholar
  8. Caro T, Sherratt TN, Stevens M (2016) The ecology of multiple colour defences. Evol Ecol 30:797–809CrossRefGoogle Scholar
  9. Cooper WE (1998) Evaluation of swab and related tests as a bioassay for assessing responses by squamate reptiles to chemical stimuli. J Chem Ecol 24:841–866CrossRefGoogle Scholar
  10. Cuthill IC, Partridge JC, Bennett AT, Church SC, Hart NS, Hunt S (2000) Ultraviolet vision in birds. Adv Study Behav 29:159–214CrossRefGoogle Scholar
  11. Deeb SS (2010) Visual pigments and colour vision in marsupials and monotremes. In: Deakin JE, Waters PD, Marshall Graves JA (eds) Marsupial genetics and genomics. Springer, Dordrecht, pp 403–414CrossRefGoogle Scholar
  12. Douglas RH, Jeffery G (2014) The spectral transmission of ocular media suggests ultraviolet sensitivity is widespread among mammals. Proc R Soc B 281:20132995–20132995CrossRefPubMedGoogle Scholar
  13. Dutson G, Dutson L (2016) Microhabitat niche differentiation in sympatric eastern blue-tongued lizard Tiliqua scincoides and blotched blue-tongued lizard Tiliqua nigrolutea in Melbourne, Victoria. Vic Nat 133:55–58Google Scholar
  14. Edmunds M (1974) Defence in animals: a survey of anti-predator defences. Longman, HarlowGoogle Scholar
  15. Endler JA, Mielke PW (2005) Comparing entire colour patterns as birds see them. Biol J Linn Soc 86:405–431CrossRefGoogle Scholar
  16. Fitzsimons JA (2011) Predation on a blotched bluetongue lizard (Tiliqua nigrolutea) by a highlands copperhead (Austrelaps ramsayi) in the Blue Mountains, Australia. Herpetol Notes 4:259–260Google Scholar
  17. 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
  18. Font E, Carazo P, Pérez i de Lanuza G, Kramer M (2012) Predator-elicited foot shakes in wall lizards (Podarcis muralis): evidence for a pursuit-deterrent function. J Comp Psychol 126:87–96CrossRefPubMedGoogle Scholar
  19. Gove D (1979) A comparative study of snake and lizard tongue-flicking, with an evolutionary hypothesis. Ethology 51:58–76Google Scholar
  20. Hart NS (2001) The visual ecology of avian photoreceptors. Prog Retin Eye Res 20:675–703CrossRefPubMedGoogle Scholar
  21. Hart NS (2002) Vision in the peafowl (Aves: Pavo cristatus). J Exp Biol 205:3925–3935PubMedGoogle Scholar
  22. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363CrossRefPubMedGoogle Scholar
  23. Humphries DA, Driver PM (1970) Protean defence by prey animals. Oecologia 5:285–302CrossRefPubMedGoogle Scholar
  24. Koenig J, Shine R, Shea G (2001) The ecology of an Australian reptile icon: how do blue-tongued lizards (Tiliqua scincoides) survive in suburbia? Wildl Res 28:215–227CrossRefGoogle Scholar
  25. Leal M, Fleishman LJ (2004) Differences in visual signal design and detectability between allopatric populations of Anolis lizards. Am Nat 163:26–39CrossRefPubMedGoogle Scholar
  26. Loew ER, Fleishman LJ, Foster RG, Provencio I (2002) Visual pigments and oil droplets in diurnal lizards. J Exp Biol 205:927–938PubMedGoogle Scholar
  27. Maan ME, Cummings ME (2012) Poison frog colors are honest signals of toxicity, particularly for bird predators. Am Nat 179:E1–E14CrossRefPubMedGoogle Scholar
  28. Maia R, Eliason CM, Bitton PP, Doucet SM, Shawkey MD (2013) Pavo: an R package for the analysis, visualization and organization of spectral data. Methods Ecol Evol 4:906–913Google Scholar
  29. Murray K, Bull CM (2004) Aggressiveness during monogamous pairing in the sleepy lizard, Tiliqua rugosa: a test of the mate guarding hypothesis. Acta Ethol 7:19–27CrossRefGoogle Scholar
  30. Nielsen TP, Bull CM (2016) Impact of foxes digging for the pygmy bluetongue lizard (Tiliqua adelaidensis). Trans R Soc S Aust 140:228–233Google Scholar
  31. Olsen J, Judge D, Fuentes E, Rose AB, Debus SJS (2010) Diets of wedge-tailed eagles (Aquila audax) and little eagles (Hieraaetus morphnoides) breeding near Canberra. J Raptor Res 44:50–61CrossRefGoogle Scholar
  32. Pérez i de Lanuza G, Carazo P, Font E (2014) Colours of quality: structural (but not pigment) coloration informs about male quality in a polychromatic lizard. Anim Behav 90:73–81CrossRefGoogle Scholar
  33. Price-Rees SJ, Brown GP, Shine R (2013) Spatial ecology of bluetongue lizards (Tiliqua spp.) in the Australian wet-dry tropics. Austral Ecology 38:493–503CrossRefGoogle Scholar
  34. Prum RO, Torres R (2003) Structural colouration of avian skin: convergent evolution of coherently scattering dermal collagen arrays. J Exp Biol 206:2409–2429CrossRefPubMedGoogle Scholar
  35. Pyron RA, Burbrink FT, Wiens JJ (2013) A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol Biol 13:93CrossRefPubMedPubMedCentralGoogle Scholar
  36. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  37. R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna Google Scholar
  38. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675CrossRefPubMedPubMedCentralGoogle Scholar
  39. Schwenk K (1995) Of tongues and noses: chemoreception in lizards and snakes. Trends Ecol Evol 10:7–12CrossRefPubMedGoogle Scholar
  40. Shine R, Phillips B, Waye H, LeMaster M, Mason RT (2003) Chemosensory cues allow courting male garter snakes to assess body length and body condition of potential mates. Behav Ecol Sociobiol 54:162–166Google Scholar
  41. Skelhorn J, Holmes GG, Rowe C (2016) Deimatic or aposematic? Anim Behav 113:e1–e3CrossRefGoogle Scholar
  42. Speed MP, Ruxton GD (2007) How bright and how nasty: explaining diversity in warning signal strength. Evolution 61:623–635CrossRefPubMedGoogle Scholar
  43. Stuart-Fox DM, Whiting MJ, Moussalli A (2006) Camouflage and colour change: antipredator responses to bird and snake predators across multiple populations in a dwarf chameleon. Biol J Linn Soc 88:437–446CrossRefGoogle Scholar
  44. Umbers KDL, Mappes J (2015) Postattack deimatic display in the mountain katydid, Acripeza reticulata. Anim Behav 100:68–73CrossRefGoogle Scholar
  45. Umbers KDL, Mappes J (2016) Towards a tractable working hypothesis for deimatic displays. Anim Behav 113:e5–e7CrossRefGoogle Scholar
  46. Umbers KDL, Lehtonen J, Mappes J (2015) Deimatic displays. Curr Biol 25:58–59CrossRefGoogle Scholar
  47. Umbers KDL, De Bonna S, White TE, Lehtonen J, Mappes J, Endler JA (2017) Deimatism: a neglected dimension of anti-predator defense. Biol Lett 13:20160936CrossRefPubMedPubMedCentralGoogle Scholar
  48. Vallin A, Jakobsson S, Lind J, Wiklund C (2005) Prey survival by predator intimidation: an experimental study of peacock butterfly defence against blue tits. Proc R Soc Lond B 272:1203–1207CrossRefGoogle Scholar
  49. Vorobyev M, Osorio D, Bennett AT, Marshall NJ, Cuthill IC (1998) Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol A 183:621–633CrossRefPubMedGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Arnaud Badiane
    • 1
    • 2
  • Pau Carazo
    • 2
  • Samantha J. Price-Rees
    • 3
  • Manuel Ferrando-Bernal
    • 2
  • Martin J. Whiting
    • 1
    Email author
  1. 1.Department of Biological SciencesMacquarie UniversitySydneyAustralia
  2. 2.Ethology lab, Cavanilles Institute of Biodiversity and Evolutionary BiologyUniversity of ValenciaValenciaSpain
  3. 3.School of Biological Sciences A08University of SydneySydneyAustralia

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