Skip to main content

Why is the tongue of blue-tongued skinks blue? Reflectance of lingual surface and its consequences for visual perception by conspecifics and predators

Abstract

Blue-tongued skinks of the genus Tiliqua (Scincidae) are characterized by their large blue melanin-pigmented tongues, often displayed during open-mouth threats, when the animal feels endangered. It is not clear whether this unusual coloration is a direct anti-predation adaptation or it may rather serve intraspecific communication, as ultraviolet-blue color is a frequent visual signal in a number of lizard species. We used spectrophotometry and visual modeling to compare blue tongues of Tiliqua gigas with tongues and skin coloration of other lizard species, and to examine their appearance through the eyes of both the conspecifics and avian predators. Our results show that (1) the tongue coloration is probably not substantially influenced by the amount of melanin in the skin, (2) lingual and oral tissues are UV-reflective in general, with blue colored tongues having chromatic qualities similar to UV-blue skin patches of other lizard species, (3) UV-blue tongues are more conspicuous than pink tongues, especially in the visual model of conspecifics. We hypothesize that blue tongues may possibly serve as a semantic (honest) signal analogous to UV-blue skin patches of other lizard species due to greater UV-bias in the vision of diurnal lizards. Regarding the social behavior and high aggressiveness in Tiliqua and their relatives, such signal might serve, e.g., in intraspecific long-distance communication between conspecifics in order to avoid aggression, and its anti-predation effect may only be a secondary function (exaptation).

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Abbate F, Latella G, Montalbano G, Guerrera MC, Germana GP, Levanti MB (2009) The lingual dorsal surface of the blue-tongue skink (Tiliqua scincoides). Anat Histol Embryol 38(5):348–350

    CAS  Article  PubMed  Google Scholar 

  • Andersson S, Örnborg J, Andersson M (1998) Ultraviolet sexual dimorphism and assortative mating in blue tits. P Roy Soc Lond B 265:445–450

    Article  Google Scholar 

  • Aumann T (2001) An intraspecific and interspecific comparison of raptor diets in the south-west of the Northern Territory, Australia. Wildlife Res 28(4):379–393

    Article  Google Scholar 

  • Ayala-Varela FP, Omar TC (2010) A new species of dactyloid anole (Iguanidae, Polychrotinae, Anolis) from the southeastern slopes of the Andes of Ecuador. Zookeys 53:59–73

    Article  PubMed  Google Scholar 

  • Bagnara JT, Fernandez PJ, Fujii R (2007) On the blue coloration of vertebrates. Pigm Cell Res 20(1):14–26

    CAS  Article  Google Scholar 

  • Bajer K, Molnár O, Török J, Herczeg G (2011) Ultraviolet nuptial color determines fight success in male European green lizards (Lacerta viridis). Biol Lett 7:866–868

    PubMed Central  Article  PubMed  Google Scholar 

  • Brown D (2012) A guide to Australian skinks in captivity. ABK/Reptile, Burleigh

    Google Scholar 

  • Burkhardt D (1989) UV vision: a bird’s eye view of feathers. J Comp Physiol A 164:787–796

    Article  Google Scholar 

  • Bustard HR (1964) Defensive behavior shown by Australian geckos, genus Diplodactylus. Herpetologica 20(3):198–200

    Google Scholar 

  • Carpenter CC, Murphy JB (1978) Tongue display by the common bluetongue (Tiliqua scincoides) Reptilia, Lacertilia, Scincidae. J Herpetol 12(3):428–429

    Article  Google Scholar 

  • Cassey P, Ewen JG, Marshall NJ, Vorobyev M, Blackburn TM, Hauber ME (2009) Are avian eggshell colors effective intraspecific communication signals in the Muscicapoidea? A perceptual modelling approach. Ibis 151:689–698

    Article  Google Scholar 

  • 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(1):145–180

    Article  Google Scholar 

  • Cogger HG (2014) Reptiles and amphibians of Australia, 7th edn. Csiro, Sydney

    Google Scholar 

  • Couldridge VC, Alexander GJ (2002) Color patterns and species recognition in four closely related species of Lake Malawi cichlid. Behav Ecol 13(1):59–64

    Article  Google Scholar 

  • Creel S, Creel NM (2002) The African wild dog: behavior, ecology, and conservation. Princeton University Press, Princeton

    Google Scholar 

  • Deeb SS (2010) Visual pigments and colour vision in marsupials and monotremes. In: Deakin JE, Waters PD, Graves JAM (eds) Marsupial genetics and genomics. Springer, Dordrecht, pp 403–414

    Chapter  Google Scholar 

  • Endler JA (1990) On the measurement and classification of colour in studies of animal colour patterns. Biol J Linn Soc 41:315–352

    Article  Google Scholar 

  • Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:S125–S153

    Article  Google Scholar 

  • Endler JA, Mielke PW (2005) Comparing entire color patterns as birds see them. Biol J Linn Soc 86:405–431

    Article  Google Scholar 

  • Fenner AL, Pavey CR, Bull CM (2012) Behavioural observations and use of burrow systems by an endangered Australian arid-zone lizard, Slater’s skink (Liopholis slateri). Aust J Zool 60(2):127–132

    Article  Google Scholar 

  • Fernald RD, Hirata NR (1977) Field study of Haplochromis burtoni: quantitative behavioural observations. Anim Behav 25:964–975

    Article  Google Scholar 

  • Fitzsimons JA (2011) Predation on a blotched bluetongue lizard (Tiliqua nigrolutea) by a Highlands copperhead (Austrelaps ramsayi) in the Blue Mountains, Australia. Herpetol Notes 4:259–260

    Google Scholar 

  • Fleay D (1950) Goannas: giant lizards of the Australian bush. Anim Kingdom 53:92–96

    Google Scholar 

  • 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 Biol Sci 278:2891–2899

    PubMed Central  Article  PubMed  Google Scholar 

  • Fleishman LJ, Loew ER, Leal M (1993) Ultraviolet vision in lizards. Nature 365:397

    Article  Google Scholar 

  • Font E, Pérez I, De Lanuza G, Sampedro C (2009) Ultraviolet reflectance and cryptic sexual dichromatism in the ocellated lizard, Lacerta (Timon) lepida (Squamata: Lacertidae). Biol J Linn Soc 97:766–780

    Article  Google Scholar 

  • Gardner MG, Hugall AF, Donnellan SC, Hutchinson MN, Foster R (2008) Molecular systematics of social skinks: phylogeny and taxonomy of the Egernia group (Reptilia: Scincidae). Zool J Linn Soc 154(4):781–794

    Article  Google Scholar 

  • Godfrey SS, Bradley JK, Sih A, Bull CM (2012) Lovers and fighters in sleepy lizard land: where do aggressive males fit in a social network? Anim Behav 83:209–215

    Article  Google Scholar 

  • Gomez D (2006) AVICOL, a program to analyse spectrometric data. Last update October 2013. Free executable available at http://sites.google.com/site/avicolprogram/

  • Graves BM, Halpern M (1991) Discrimination of self from conspecific chemical cues in Tiliqua scincoides (Sauria: Scincidae). J Herpetol 25(1):125–126

    Article  Google Scholar 

  • Hamilton DG, Whiting MJ, Pryke SR (2013) Fiery frills: carotenoid-based coloration predicts contest success in frillneck lizards. Behav Ecol 24(5):1138–1149

    Article  Google Scholar 

  • Hart NS (2002) Vision in the peafowl (Aves: Pavo cristatus). J Exp Biol 205:3925–3935

    PubMed  Google Scholar 

  • Hart NS, Coimbra JP, Collin SP, Westhoff G (2012) Photoreceptor types, visual pigments, and topographic specializations in the retinas of hydrophiid sea snakes. J Comp Neurol 520(6):1246–1261

    CAS  Article  PubMed  Google Scholar 

  • Håstad O, Victorsson J, Ödeen A (2005) Differences in color vision make passerines less conspicuous in the eyes of their predators. PNAS 102(18):6391–6394

    PubMed Central  Article  PubMed  Google Scholar 

  • Hauschild A, Hitz R, Henle K, Shea GM, Werning H (2000) Blauzungenskinke, Beiträge zu Tiliqua und Cyclodomorphus. Natur und Tier, Münster

    Google Scholar 

  • Herrel A (2000) Die Funktion der Zungenfärbung bei Blauzungenskinken (Tiliqua spp.). In: Hauschild A, Hitz R, Shea G, Werning H (eds) Blauzungenskinke, Beiträge zu Tiliqua und Cyclodomorphus. Natur und Tier, Münster, pp 27–30

    Google Scholar 

  • Hill GE, McGraw KJ (2006) Bird coloration: function and evolution. Harvard University Press, Cambridge

    Google Scholar 

  • Holáňová V, Rehák I, Frynta D (2012) Anolis sierramaestrae sp. nov. (Squamata: Polychrotidae) of the “chamaeleolis” species group from Eastern Cuba. Acta Soc Zool Bohem 76:45–52

    Google Scholar 

  • Hunt S, Kilner RM, Langmore NE, Bennett ATD (2003) Conspicuous, ultraviolet-rich mouth colors in begging chicks. Proc R Soc Lond B 270:25–28

    Article  Google Scholar 

  • Hutchinson MN, Milne T, Croft T (1994) Redescription and ecological notes on the pygmy bluetongue, Tiliqua adelaidensis (Squamata: Scincidae). T Roy Soc South Aust 118(4):217–226

    Google Scholar 

  • Jawor JM, Breitwisch R (2003) Melanin ornaments, honesty, and sexual selection. Auk 120(2):249–265

    Article  Google Scholar 

  • Jourdie V, Moureau B, Bennett ATD, Heeb P (2004) Ultraviolet reflectance by the skin of nestlings. Nature 431:262

    CAS  Article  PubMed  Google Scholar 

  • Kerr GD, Bull MD (2006) Exclusive core areas in overlapping ranges of the sleepy lizard, Tiliqua rugosa. Behav Ecol 17(3):380–391

    Article  Google Scholar 

  • Koenig J, Shine R, Shea G (2002) The dangers of life in the city: patterns of activity, injury and mortality in suburban lizards (Tiliqua scincoides). J Herpetol 36(1):62–68

    Article  Google Scholar 

  • Landová E, Jančúchová-Lásková J, Musilová V, Kadochová Š, Frynta D (2013) Ontogenetic switch between alternative antipredatory strategies in the leopard gecko (Eublepharis macularius): defensive threat versus escape. Behav Ecol Sociobiol 67(7):1113–1122

    Article  Google Scholar 

  • Langkilde T, Shine R (2005) How do water skinks avoid shelters already occupied by other lizards? Behaviour 142(2):203–216

    Article  Google Scholar 

  • Lind O, Mitkus M, Olsson P, Kelber A (2013) Ultraviolet sensitivity and color vision in raptor foraging. J Exp Biol 216(10):1819–1826

    Article  PubMed  Google Scholar 

  • Loew ER (1994) A third, ultraviolet-sensitive, visual pigment in the Tokay gecko (Gekko gekko). Vision Res 34(11):1427–1431

    CAS  Article  PubMed  Google Scholar 

  • Loew ER, Fleishman LJ, Foster RG, Provencio I (2002) Visual pigments and oil droplets in diurnal lizards: a comparative study of Caribbean anoles. J Exp Biol 205:927–938

    PubMed  Google Scholar 

  • Loew ER, Govardovskii VI, Röhlich P, Szel A (1996) Microspectrophotometric and immunocytochemical identification of ultraviolet photoreceptors in geckos. Visual Neurosci 13(02):247–256

    CAS  Article  Google Scholar 

  • Losos JB (1985) An experimental demonstration of the species-recognition role of Anolis dewlap color. Copeia 1985(4):905–910

    Article  Google Scholar 

  • Lyytinen A, Alatalo RV, Lindström L, Mappes J (2001) Can ultraviolet cues function as aposematic signals? Behav Ecol 12(1):65–70

    Article  Google Scholar 

  • Macedonia JM, Lappin AK, Loew ER, Mcguire JA, Hamilton PS, Plasman M, Brandt Y, Lemos-Espinal JA, Kemp DJ (2009) Conspicuousness of Dickerson’s collared lizard (Crotaphytus dickersonae) through the eyes of conspecifics and predators. Biol J Linn Soc 97:749–765

    Article  Google Scholar 

  • Mafli A, Wakamatsu K, Roulin A (2011) Melanin-based coloration predicts aggressiveness and boldness in captive eastern Hermann’s tortoises. Anim Behav 81:859–863

    Article  Google Scholar 

  • Main AR, Bull MC (1996) Mother–offspring recognition in two Australian lizards, Tiliqua rugosa and Egernia stokesii. Anim Behav 52:193–200

    Article  Google Scholar 

  • Mann SL, Meek R (2004) Understanding the relationship between body temperature and activity patterns in the giant Solomon Island skink, Corucia zebrata, as a contribution to the effectiveness of captive breeding programmes. Appl Herpetol 1(3):287–298

    Article  Google Scholar 

  • Marshall KLA, Stevens M (2014) Wall lizards display conspicuous signals to conspecifics and reduce detection by avian predators. Behav Ecol 25(6):1325–1337

    PubMed Central  Article  PubMed  Google Scholar 

  • Martin M, Le Galliard JF, Meylan S, Loew ER (2015) The importance of short and near infrared wavelength sensitivity for visual discrimination in two species of lacertid lizards. J Exp Biol 218:458–465

    Article  PubMed  Google Scholar 

  • Mayes PJ, Thompson GG, Withers PC (2005) Diet and foraging behaviour of the semi-aquatic Varanus mertensi (Reptilia: Varanidae). Wildlife Res 32(1):67–74

    Article  Google Scholar 

  • McDonald PG, Olsen PD, Baker-Gabb DJ (2003) Territory fidelity, reproductive success and prey choice in the brown falcon, Falco berigora: a flexible bet-hedger? Aust J Zool 51(4):399–414

    Article  Google Scholar 

  • McGraw KJ, Dale J, Mackillop EA (2003) Social environment during molt and the expression of melanin-based plumage pigmentation in male house sparrows (Passer domesticus). Behav Ecol Sociobiol 53:116–122

    Google Scholar 

  • McGraw KJ, Safran RJ, Wakamatsu K (2005) How feather colour reflects its melanin content. Funct Ecol 19(5):816–821

    Article  Google Scholar 

  • Melville J, Schulte JA, Larson A (2004) A molecular study of phylogenetic relationships and evolution of antipredator strategies in Australian Diplodactylus geckos, subgenus Strophurus. Biol J Linn Soc 82(1):123–138

    Article  Google Scholar 

  • Miller EJ, Herbert CA (2010) Breeding and genetic management of captive marsupial populations. In: Deakin JE, Waters PD, Graves JAM (eds) Marsupial genetics and genomics. Springer, Dordrecht, pp 5–32

    Chapter  Google Scholar 

  • Molina-Borja M, Font E, Mesa-Avila G (2006) Sex and population variation in ultraviolet reflectance of color patches in Gallotia galloti (fam. Lacertidae) from Tenerife (Canary Islands). J Zool 268:193–206

    Article  Google Scholar 

  • Murray KC, Bull M (2004) Aggressiveness during monogamous pairing in the sleepy lizard, Tiliqua rugosa: a test of the mate guarding hypothesis. Acta Herpetol 7(1):19–27

    Google Scholar 

  • New ST, Hemmi JM, Kerr GD, Bull CM (2012) Ocular anatomy and retinal photoreceptors in a skink, the sleepy lizard (Tiliqua rugosa). Anat Rec 295(10):1727–1735

  • Ödeen A, Håstad O (2003) Complex distribution of avian color vision systems revealed by sequencing the SWS1 opsin from total DNA. Mol Biol Evol 20:855–861

    Article  PubMed  Google Scholar 

  • Ödeen A, Håstad O (2013) The phylogenetic distribution of ultraviolet sensitivity in birds. BMC Evol Biol 13(1):36

    PubMed Central  Article  PubMed  Google Scholar 

  • 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, Australia. J Raptor Res 44(1):50–61

    Article  Google Scholar 

  • Perez I, De Lanuza G, Carazo P, Font E (2014a) Colors of quality: structural (but not pigment) coloration informs about male quality in a polychromatic lizard. Anim Behav 90:73–81

    Article  Google Scholar 

  • Perez I, De Lanuza G, Font E (2010) Lizard blues: blue body coloration and ultraviolet polychromatism in lacertids. Rev Esp Herpetol 24:67–84

    Google Scholar 

  • Perez I, De Lanuza G, Font E (2014b) Now you see me, now you don’t: iridescence increases the efficacy of lizard chromatic signals. Naturwissenschaften 101:831–837

  • Perez I, De Lanuza G, Font E (2014c) Ultraviolet vision in lacertid lizards: evidence from retinal structure, eye transmittance, SWS1 visual pigment genes and behaviour. J Exp Biol 217(16):2899–2909

  • Plasman M, Reynoso VH, Nicolás L, Torres R (2015) Multiple color traits signal performance and immune response in the Dickerson’s collared lizard Crotaphytus dickersonae. Behav Ecol Soc 69:765–775

    Article  Google Scholar 

  • Price-Rees SJ, Brown GP, Shine R (2012) Spatial ecology of bluetongue lizards (Tiliqua spp.) in the Australian wet–dry tropics. Aust Ecol 38:493–503

    Article  Google Scholar 

  • Price-Rees SJ, Brown GP, Shine R (2013) Habitat selection by bluetongue lizards (Tiliqua, Scincidae) in tropical Australia: a study using GPS telemetry. Anim Biotelemetry 1:1–14

    Article  Google Scholar 

  • Price-Rees SJ, Brown GP, Shine R (2014) Activity Patterns and Movements of Free-Ranging Bluetongue Lizards (Tiliqua scincoides intermedia and Tiliqua multifasciata) in the Australian Wet-Dry Tropics. J Herpetol 48(3):298–305

    Article  Google Scholar 

  • Pyron RA, Burbrink FT, Wiens JJ (2013) A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol Biol 13:93

    PubMed Central  Article  PubMed  Google Scholar 

  • Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, Oxford

    Book  Google Scholar 

  • Senar JC (2006) Color displays as intrasexual signals of aggression and dominance. In: Hill GE, McGraw KJ (eds) Bird coloration: function and evolution. Harvard University Press, Cambridge, pp 87–136

    Google Scholar 

  • Shea G, Amey A, Couper P (2005) Fatal intra-specific aggression in free ranging blue tongued lizards, Tiliqua scincoides (Scincidae). Herpetofauna 35(2):73–75

    Google Scholar 

  • Shea GM (1995) A taxonomic revision of the Cyclodomorphus casuarinae complex (Squamata: Scincidae). Rec Aust Mus 47:83–115

    Article  Google Scholar 

  • Shea GM (2006) Diet of two species of bluetongue skink, Tiliqua multifasciata and Tiliqua occipitalis (Squamata: Scincidae). Aust Zoologist 33(3):359–368

    Article  Google Scholar 

  • Shea GM, Miller B (1995) A Taxonomic revision of the Cyclodomorphus branchialis species group (Squamata: Scincidae). Rec Aust Mus 47:265–325

    Article  Google Scholar 

  • Sherbrooke WC (1991) Behavioral (predator-prey) interactions of captive grasshopper mice (Onychomys torridus) and horned lizards (Phrynosoma cornutum and P. modestum). Am Midl Nat 126(1):187–195

    Article  Google Scholar 

  • Shine R, Keogh JS (1996) Food habits and reproductive biology of the endemic Melanesian elapids: are tropical snakes really different? J Herpetol 30(2):238–247

    Article  Google Scholar 

  • Shriver MD, Parra EJ (2000) Comparison of narrow-band reflectance spectroscopy and tristimulus colorimetry for measurements of skin and hair color in persons of different biological ancestry. Am J Phys Anthropol 112(1):17–27

    CAS  Article  PubMed  Google Scholar 

  • Siddiqi A, Cronin TW, Loew ER, Vorobyev M, Summers K (2004) Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio. J Exp Biol 207:2471–2485

    Article  PubMed  Google Scholar 

  • Sillman AJ, Govardovskii VI, Röhlich P, Southard JA, Loew ER (1997) The photoreceptors and visual pigments of the garter snake (Thamnophis sirtalis): a microspectrophotometric, scanning electron microscopic and immunocytochemical study. J Comp Physiol A 181(2):89–101

    CAS  Article  PubMed  Google Scholar 

  • Sillman AJ, Johnson JL, Loew ER (2001) Retinal photoreceptors and visual pigments in Boa constrictor imperator. J Exp Zool 290(4):359–365

    CAS  Article  PubMed  Google Scholar 

  • Sillman AJ, Carver JK, Loew ER (1999) The photoreceptors and visual pigments in the retina of a boid snake, the ball python (Python regius). J Exp Biol 202(14):1931–1938

    PubMed  Google Scholar 

  • Sinervo B, Miles DB, Frankino WA, Klukowski M, DeNardo DF (2000) Testosterone, endurance, and Darwinian fitness: natural and sexual selection on the physiological bases of alternative male behaviors in side-blotched lizards. Horm Behav 38(4):222–233

    CAS  Article  PubMed  Google Scholar 

  • StatSoft, Inc. (2007). STATISTICA (data analysis software system), version 8.0. www.statsoft.com

  • Stoddard MC, Prum RO (2008) Evolution of avian plumage color in a tetrahedral color space: a phylogenetic analysis of new world buntings. Am Nat 171:755–776

    Article  PubMed  Google Scholar 

  • Umbers KD (2013) On the perception, production and function of blue colouration in animals. J Zool 289(4):229–242

    Article  Google Scholar 

  • Vitt LJ, Lacher TE (1981) Behavior, habitat, diet, and reproduction of the iguanid lizard Polychrus acutirostris in the caatinga of northeastern Brazil. Herpetologica 37(1):53–63

    Google Scholar 

  • Vorobyev M, Osorio D (1998) Receptor noise as a determinant of color thresholds. Proc R Soc Lond B 265:351–358

    CAS  Article  Google Scholar 

  • Vorobyev M, Osorio D, Bennett ATD, Marshall NJ, Cuthill IC (1998) Tetrachromacy, oil droplets and bird plumage colors. J Comp Physiol 183(5):621–633

    CAS  Article  Google Scholar 

  • Whiting MJ, Stuart-Fox DM, O’Connor D, Firth D, Bennett NC, Blomberg SP (2006) Ultraviolet signals ultra-aggression in a lizard. Anim Behav 72:353–363

    Article  Google Scholar 

  • Williams EE, Rand AS (1977) Species recognition, dewlap function and faunal size. Am Zool 17(1):261–270

    Google Scholar 

Download references

Acknowledgements

We thank Leo Fleishman for kindly providing photoreceptor data for P. broadleyi, Tomáš Grim and Dan Hanley for lending the spectrophotometer, Veronika Holáňová (Hříbalová) and Tomáš Protiva for providing C. zebrata and C. gerrardii. The work was supported by Grant Agency of Charles University in Prague (project No. 754213).

Ethical standards

This study was allowed by Ethical Committee of the Charles University in Prague, Czech Republic and approved by Ethical Committee of Ministry of Education, Youth and Sports, license no. 26582/2012-30.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniel Frynta.

Additional information

Communicated by: Sven Thatje

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Abramjan, A., Bauerová, A., Somerová, B. et al. Why is the tongue of blue-tongued skinks blue? Reflectance of lingual surface and its consequences for visual perception by conspecifics and predators. Sci Nat 102, 42 (2015). https://doi.org/10.1007/s00114-015-1293-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00114-015-1293-4

Keywords

  • Coloration
  • Signaling
  • Lizards
  • Evolution
  • Tiliqua