Abstract
One physiological mechanism used by reptiles to remain within thermal optima is their ability to reversibly alter skin colour, imparting changes in overall reflectance, and influencing the rate of heat gain from incident radiation. The ability to lighten or darken their skin is caused by the movement of pigment within the dermal chromatophore cells. Additionally, lizards, as ectotherms, significantly lower their preferred body temperatures when experiencing stressors such as hypoxia. This decrease in preferred temperature has been proposed to be the result of a downward adjustment of the thermal set-point, the temperature around which the body temperature is typically defended. We tested the hypothesis that lightening of the skin in lizards would be modified by hypoxia in a manner consistent with the known reduction in preferred temperatures. Skin colouration values of the dorsal skin of bearded dragons were analysed at three different levels of oxygen (20.8, 9.9 and 4.9 kPa) and at temperatures spanning the preferred temperature range (30, 32, 34, 36, 38 and 40 C). Hypoxic lizards lightened their skin at lower ambient temperatures more than normoxic ones, and in an oxygen-dependent fashion. The orchestrated adjustment of skin reflectance suggests that this physiological trait is being regulated at a new and lower set-point. Evidence from this study demonstrates that skin colouration plays a role in body temperature regulation and that the reduction in temperature set-point so prevalent in hypoxia is also manifested in this physiological trait.
Similar content being viewed by others
References
Bagnara JT, Hadley ME (1973) Chromatophores and color change: the comparative physiology of animal pigmentation. Prentice-Hall, Eaglewood Cliffs
Bagnara JT, Taylor JD, Hadley ME (1968) Dermal chromatophore unit. J Cell Biol 38:67–79
Barber BJ, Crawford EC (1979) Dual threshold control of peripheral temperature in the Lizard Dipsosaurus dorsalis. Physiol Zool 52:250–263
Bartholomew GA (1982) Physiological control of body temperature. In: Gans C, Pough FH (eds) Biology of the Reptilia. Academic Press, London, pp 167–211
Bartholomew GA, Tucker VA (1963) Control of changes in body temperature, metabolism, and circulation by the agamid lizard, Amphibolurus barbatus. Physiol Zool 36:199–218
Carey C (1978) Factors affecting body temperatures of toads. Oecologia 35:197–219
Christian KA (1998) Thermoregulation by the short-horned lizard (Phrynosoma douglassi) at high elevation. J Therm Biol 23:395–399
Cole LC (1943) Experiments on toleration of high temperature in lizards with reference to adaptive coloration. Ecology 24:94–108
Drimbarean A, Whelan PF (2001) Experiments in colour texture analysis. Pattern Recognit Lett 22:1161–1167
Greenberg N (2002) Ethological aspects of stress in a model lizard, Anolis carolinensis. Int Comp Biol 42:526–540
Hadley ME (1972) Functional significance of vertebrate integumental pigmentation. Am Zool 12:63–76
Hicks JW, Wood SC (1985) Temperature regulation in lizards: effects of hypoxia. Am J Physiol 248:R595–R600
Iga T, Bagnara JT (1975) Analysis of color change phenomena in leaf frog, Agalychnis dacnicolor. J Exp Zool 192:331–341
King RB, Hauff S, Phillips JB (1994) Physiological color change in the green treefrog. Responses to background brightness and temperature. Copeia 2:422–432
Lutterschmidt WI, Lutterschmidt DI, Tracy CR, Hutchison VH (1998) Time course analyses of the thermoregulatory responses to melatonin and chlorpromazine in bull snakes (Pituophis melanoleucus). J Therm Biol 23:319–327
Oshima N (2001) Direct reception of light by chromatophores of lower vertebrates. Pigment Cell Res 14:312–319
Pearson OP (1977) Effect of substrate and of skin color on thermoregulation of a lizard. Comp Biochem Physiol A 58:353–358
Pörtner H-O, Branco LGS, Malvin GM, Wood SC (1994) A new function for lactate in the toad Bufo marinus. J Appl Physiol 76:2405–2410
Rahn H (1956) The relationship between hypoxia, temperature, adrenalin release and melanophore expansion in the lizard, Anolis caroliniensis. Copeia 1956:214–217
Sherbrooke WC (1997) Physiological (rapid) change of color in horned lizards (Phrynosoma) of arid habitats: hormonal regulation, effects of temperature, and role in nature. Amphib-reptil 18:155–175
Sherbrooke WC, Castrucci AMD, Hadley ME (1994) Temperature effects on in vitro skin darkening in the mountain spiny lizard, Sceloporus jarrovii—a thermoregulatory adaptation. Physiol Zool 67:659–672
Sherbrooke WC, Frost SK (1989) Integumental chromatophores of a color-change, thermoregulating lizard, Phrynosoma modestum (Iguanidae; Reptilia). Am Mus Novit 2943:1–14
Stuart-Fox DM, Moussalli A, Johnston GR, Owens IPF (2004) Evolution of color variation in dragon lizards: quantitative tests of the role of crypsis and local adaptation. Evolution 58:1549–1559
Tattersall GJ, Eterovick PC, de Andrade DV (2006) Tribute to R.G. Boutilier: skin colour and body temperature changes in basking Bokermannohyla alvarengai (Bokermann 1956). J Exp Biol 209:1185–1196
Tattersall GJ, Gerlach RM (2005) Hypoxia progressively lowers thermal gaping thresholds in bearded dragons, Pogona vitticeps. J Exp Biol 208:3321–3330
Vaughan GL, Greenberg N (1987) Propanolol, a beta-adrenergic antagonist, retards response to MSH in skin of Anolis carolinensis. Physiol Behav 40:555–558
Walton BM, Bennett AF (1993) Temperature-dependent color-change in Kenyan chameleons. Physiol Zool 66:270–287
Wood SC, Gonzales R (1996) Hypothermia in hypoxic animals: mechanisms, mediators, and functional significance. Comp Biochem Physiol B 113:37–43
Acknowledgments
The authors would like to acknowledge Christopher Loewen, Viviana Cadena, and Matthew Skinner for valuable assistance with experiments, and Tom Eles for providing the essential animal care. The research was conducted as part of Brock University’s Biological Sciences BSc. Honours Thesis program (JBV) and was funded by the Natural Sciences and Engineering Research Council of Canada and the Canadian Foundation for Innovation to GJT. Experimental procedures were approved by Brock University’s Animal Care and Use Committee (AUPP #03-10-01).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by H.V. Carey.
Rights and permissions
About this article
Cite this article
de Velasco, J.B., Tattersall, G.J. The influence of hypoxia on the thermal sensitivity of skin colouration in the bearded dragon, Pogona vitticeps . J Comp Physiol B 178, 867–875 (2008). https://doi.org/10.1007/s00360-008-0274-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-008-0274-8