Zheng WANG,Hongliang LU,Li MA and Xiang JI.Differences in Thermal Preference and Tolerance among Three Phrynocephalus Lizards (Agamidae) with Different Body Sizes and Habitat Use[J].Asian Herpetological Research(AHR),2013,4(3):214-220.[doi:10.3724/SP.J.1245.2013.000214]
Click Copy

Differences in Thermal Preference and Tolerance among Three Phrynocephalus Lizards (Agamidae) with Different Body Sizes and Habitat Use
Share To:

Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]

2013 VoI.4 No.3
Research Field:
Original Article
Publishing date:


Differences in Thermal Preference and Tolerance among Three Phrynocephalus Lizards (Agamidae) with Different Body Sizes and Habitat Use
Zheng WANG12 Hongliang LU3 Li MA3 and Xiang JI2*
1 College of Forest Resources and Environment, Nanjing Forestry University, Nanjing 210037, Jiangsu, China
2 Jiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210046, Jiangsu, China
3 Hangzhou Key Laboratory for Animal Adaptation and Evolution, School of Life Sciences, Hangzhou Normal University, Hangzhou 310036, Zhejiang, China
Agamidae Phrynocephalus lizards thermal preference thermal tolerance body size habitat use
We acclimated adults of two viviparous (Phrynocephalus guinanensis and P. vlangalii) and one oviparous (P. versicolor) species of toad-headed lizards (Agamidae) to 28 °C, 33 °C and 38 °C to examine whether thermal preference (preferred body temperature, Tp) and thermal tolerance (critical thermal minimum, CTMin; critical thermal maximum, CTMax) were affected by acclimation temperature, and correlate with body size and habitat use. Both Tp and CTMax were highest in P. versicolor and lowest in P. vlangalii, with P. guinanensis in between. The two viviparous species did not differ in CTMin and thermal tolerance range, and they both were more resistant to low temperatures and had a wider range of thermal tolerance than the oviparous species. Both CTMin and CTMax shifted upward as acclimation temperature increased in all the three species. Tp was higher in the lizards acclimated to 33 °C than in those to 28 °C or 38 °C. The range of thermal tolerance was wider in the lizards acclimated to 28 °C than in those to 33 °C or 38 °C. The data showed that: 1) thermal preference and tolerance were affected by acclimation temperature, and differed among the three species of Phrynocephalus lizards with different body sizes and habitat uses; 2) both Tp and CTMax were higher in the species exchanging heat more rapidly with the environment, and CTMin was higher in the species using warmer habitats during the active season; and 3) thermal preference and tolerance might correlat with body size and habitat use in Phrynocephalus lizards.


Alexander C. E. 1966. Energy requirements of the side-blotched lizard, Uta stansburiana. M.S. Thesis. New Mexico State University, Las Cruces, USA
Angilletta M. J. 2009. Thermal Adaptation: A Theoretical and Empirical Synthesis. New York: Oxford University Press
Bennett A. F., John-Alder H. B. 1986. Thermal relations of some Australian skinks (Sauria: Scincidae). Copeia, 1986: 57?64
Brattstrom B. H. 1965. Body temperature of reptiles. Am Midl Nat, 73: 376–422
Brattstrom B. H. 1971. Critical thermal maxima of some Australian skinks. Copeia, 1971: 554?557
Christian K. A., Weavers B. W. 1996. Thermoregulation of monitor lizards in Australia: An evaluation of methods in thermal biology. Ecol Monogr, 66: 139?157
Corn M. J. 1971. Upper thermal limits and thermal preferenda for three sympatric species of Anolis. J Herpetol, 5: 17?21
Cruz F. B., Fitzgerald L. A., Espinoza R. E., Schulte J. A. 2005. The importance of phylogenetic scale in tests of Bergmann’s and Rapoport’s rules: Lessons from a clade of South American lizards. J Evol Biol, 18: 1559?1574
Hertz P. E., Huey R. B., Stevenson R. D. 1993. Evaluating temperature regulation by field-active ectotherms: The fallacy of the inappropriate question. Am Nat, 142: 796?818
Hochachka P. W., Somero G. N. 2002. Biochemical Adaptation: Mechanism and Process in Physiological Evolution. Philadelphia: Oxford University Press
Huang S. P., Hsu Y. Y., Tu M. C. 2006. Thermal tolerance and altitudinal distribution of two Sphenomorphus lizards in Taiwan. J Therm Biol, 31: 378?385
Huey R. B. 1982. Temperature, physiology, and the ecology of reptiles. In Gans C., Pough F. H. (Eds.), Biology of the Reptilia, Vol. 12. London: Academic Press, 25?91
Huey R. B., Slatkin M. 1976. Costs and benefits of lizard thermoregulation. Q Rev Biol, 51: 363?384
Hutchison V. H. 1961. Critical thermal maxima in salamanders. Physiol Zool, 2: 92?125
Ji X., Du W. G., Sun P. Y. 1996. Body temperature, thermal tolerance and influence of temperature on sprint speed and food assimilation in adult grass lizards, Takydromus septentrionalis. J Therm Biol, 21: 155?161
Ji X., Wang Y. Z., Wang Z. 2009. New species of Phrynocephalus (Squamata, Agamidae) from Qinghai, Northwest China. Zootaxa, 1988: 61?68
Kour E. L., Hutchison V.H. 1970. Critical thermal tolerances and heating and cooling rates of lizards from diverse habitats. Copeia, 1970: 219?229
Li H., Qu Y. F., Hu R. B., Ji X. 2009a. Evolution of viviparity in cold-climate lizards: Testing the maternal manipulation hypothesis. Evol Ecol, 23: 777?790
Li H., Wang Z., Mei W. B., Ji X. 2009b. Temperature acclimation affects thermal preference and tolerance in three Eremias lizards (Lacertidae). Curr Zool, 55: 258?265
Licht P. 1968. Response of the thermal preferendum and heat resistance to thermal acclimation under different photoperiods in the lizard Anolis carolinensis. Am Midl Nat, 79: 149?158
Lin C. X., Zhang L., Ji X. 2008. Influence of pregnancy on locomotor performances of the skink, Mabuya multifasciata: why do females shift thermal preferences when pregnant? Zoology, 111: 188?195
Lowe C. H., Vance J. H. 1955. Acclimation of the critical thermal maximum of the reptile Urosaurus ornatus. Science, 122: 73?74
Lutterschmidt W. I., Hutchison V. H. 1997. The critical thermal maximum: History and critique. Can J Zool, 75: 1561?1574
Meiri S., Bauer A., Chirio L., Colli G., Das I., Doan T., Feldman A., Herrera F. C., Novosolov M., Pafilis P., Pincheira-Donoso D., Powney G., Torres-Carvajal O., Uetz P., Van Damme R. 2013. Are lizards feeling the heat? A tale of ecology and evolution under two temperatures. Global Ecol Biogeogr, 22: 834?845
Patterson J. W. 1991. Emergence, basking behaviour, mean selected temperature and critical thermal minimum in high and low altitude subspecies of the tropical lizard Mabuya striata. Afr J Ecol, 37: 330?339
Patterson J. W., Davies P. M. C. 1978. Preferred body temperature: seasonal and sexual differences in the lizard Lacerta vivipara. J Therm Biol, 3: 39?41
Qu Y. F., Gao J. F., Mao L. X., Ji X. 2011a. Sexual dimorphism and female reproduction in two sympatric toad-headed lizards, Phrynocephalus frontalis and P. versicolor (Agamidae). Anim Biol, 61: 139?151
Qu Y. F., Li H., Gao J. F., Xu X. F., Ji X. 2011b. Thermal preference, thermal tolerance and the thermal dependence of digestive performance in two coexisting Phrynocephalus lizards (Agamidae), with a review of species studied. Curr Zool, 57: 684?700
Sagonas K., Meiri S., Valakos E. D., Pafilis P. 2013. The effect of body size on the thermoregulation of lizards on hot, dry Mediterranean islands. J Therm Biol, 38: 92?97
Sartorius S. S., do Amaral J. P. S., Durtsche R. D., Deen C. M., Lutterschmidt W. I. 2002. Thermoregulatory accuracy, precision, and effectiveness in two sand-dwelling lizards under mild environmental conditions. Can J Zool, 80: 1966?1976
Schmidt-Nielsen K. 1984. Scaling: Why is animal size so important? New York: Cambridge University Press
Shine R., Madsen T. 1996. Is thermoregulation unimportant for most reptiles? An example using water pythons Liasis fuscus in tropical Australia. Physiol Zool, 69: 252?269
Shu L., Zhang Q. L., Qu Y. F., Ji X. 2010. Thermal tolerance, selected body temperature and thermal dependence of food assimilation and locomotor performance in the Qinghai toad-headed lizard Phrynocephalus vlangalli. Acta Ecol Sin, 30: 2036?2042
Sinervo B., Méndez-de-la-Cruz F., Miles D. B., Heulin B., Bastiaans E., Villagrán-Santa C. M., Lara-Resendiz R., Martínez-Méndez N., Calderón-Espinosa M. L., Meza-Lázaro R. N., Gadsden H., Avila L. J., Morando M., De La Riva I. J., Sepulveda P. V., Rocha C. F. D., Ibargüengoytía N., Puntriano C. A., Massot M., Lepetz V., Oksanen T. A., Chapple D. G., Bauer A. M., Branch W. R., Clobert J., Sites J. W. 2010. Erosion of lizard diversity by climate change and altered thermal niches. Science, 328: 894?899
Wang Z. 2011. Adapting to extreme climate: The evolution of viviparity in Phrynocephalus lizards. Ph.D. Thesis, Nanjing Normal University, Nanjing, China
Werner Y. L., Takahashi H., Mautz W. J., Ota H. 2005. Behavior of the terrestrial nocturnal lizards Goniurosaurus kuroiwae kuroiwae and Eublepharis macularius (Reptilia: Eublepharidae) in a thigmothermal gradient. J Therm Biol, 30: 247?254
Wilhoft D. C., Anderson J. D. 1960. Effect of acclimation on the preferred body temperature of the lizard, Sceloporus occidentalis. Science, 131: 610?611
Yang J., Sun Y. Y., An H., Ji X. 2008. Northern grass lizards (Takydromus septentrionalis) from different populations do not differ in thermal preference and thermal tolerance when acclimated under identical thermal conditions. J Comp Physiol B, 178: 343?349
Zhang X. D., Ji X., Luo L. G., Gao J. F., Zhang L. 2005. Sexual dimorphism and female reproduction in the Qinghai toad-headed lizard Phrynocephalus vlangalii. Acta Zool Sin, 51: 1006?1012
Zhao K. T. 1999. Phrynocephalus Kaup. In Zhao E. M., Zhao K. T., Zhou K. Y. (Eds.), Fauna Sinica, Reptilia, Vol. 2 (Squamata: Lacertilia). Beijing: Science Press, 151?192
Sanders K. L., Lee M. S., Leys R., Foster R., Keogh J. S. 2008. Molecular phylogeny and divergence dates for Australasian elapids and sea snakes (Hydrophiinae): Evidence from seven genes for rapid evolutionary radiations. J Evol Biol, 21: 682–695
Santos X., Roca J., Pleguezuelos J. M., Donaire D., Carranza S. 2008. Biogeography and evolution of the Smooth snake Coronella austriaca (Serpentes: Colubridae) in the Iberian Peninsula: Evidence for Messinian refuges and Pleistocenic range expansions. Amphibia-Reptilia, 29: 35–47
Schaetti B., Utiger U. 2001. A new genus for Zamenis socotrae Guenther, 1881 and a contribution to the phylogeny of Old World racers, whip snakes and related genera (Reptilia: Squamata: Colubrinae). Rev Suisse Zool, 108: 919–948
Simpson G. G. 1943. Mammals and the nature of continents. Am J Sci, 241: 1–31
Tamura K., Dudley J., Nei M., Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol, 24: 1596–1599
Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. 1997. The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res, 25: 4876–4882
Thomson R. C., Wang I. J., Johnson J. R. 2010. Genome-enabled development of DNA markers for ecology, evolution and conservation. Mol Ecol, 19: 2184–2195
Uetz P. 2013. The Reptile Database [Internet]. Zoological Museum, Hamburg, Germany. Electronic database accessible at http://www.reptile-database.org
Utiger U., Helfenberger N., Sch?tti B., Schmidt C., Ruf M., Zisweiler Z. 2002. Molecular systematics and phylogeny of Old World and New World ratsnakes, Elaphe Auct., and related genera (Reptilia, Squamata, Colubridae). Russ J Herpetol, 9: 105–124
Utiger U., Schaetti B. 2004. Morphology and phylogenetic relationships of the Cyprus racer, Hierophis cypriensis, and the systematic status of Coluber gemonensis gyarosensis Mertens (Squamata, Colubrinae). Rev Suisse Zool, 111: 225–238
Vidal N., Branch W. R., Pauwels O. S. G., Hedges S. B., Broadley D. G., Wink M., Cruaud C., Joger U., Nagy Z. T. 2008. Dissecting the major African snake radiation: A molecular phylogeny of the Lamprophiidae Fitzinger (Serpentes, Caenophidia). Zootaxa, 1945: 51–66
Vidal N., Delmas A., David P., Cruaudd C., Coulouxd A., Hedgesa S. B. 2007. The phylogeny and classification of caenophidian snakes inferred from seven nuclear protein-coding genes. C R Biologies, 330: 182–187
Vidal N., Dewynter M., Gower D. J. 2010. Dissecting the major American snake radiation: A molecular phylogeny of the Dipsadidae Bonaparte (Serpentes, Caenophidia). C R Biologies, 333: 48–55
Vidal N., Hedges S. B. 2002. Higher-level relationships of snakes inferred from four nuclear and mitochondrial genes. C R Biologies, 325: 977–985
Vidal N., Kindl S. G., Wong A., Hedges S. B. 2000. Phylogenetic relationships of xenodontine snakes inferred from 12s and 16s ribosomal RNA sequences. Mol Phylogenet Evol, 14: 389–402
Wilcox T. P., Zwickl D. J., Heath T. A., Hillis D. M. 2002. Phylogenetic relationships of the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic support. Mol Phylogenet Evol, 25: 361–371
Zaher H. 1999. Hemipenial morphology of the South American xenodontine snakes, with a proposal for a monophyletic Xenodontinae and a reappraisal of colubroid hemipenes. New York: Bull Am Mus Nat Hist
Zaher H., Grazziotin F. G., Cadle J. E., Murphy R. W., Moura-Leite J. C., Bonatto S. L. 2009. Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South America xenodontines: A revised classification and descriptions of new taxa. Pap Av Zool, 49: 115–153
Zhao E. M. 2006. Snakes in China, Vol. 1. Hefei: Anhui Science and Technology Publishing House (In Chinese)
Zwickl D. J. 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. thesis, the University of Texas at Austin


Last Update: 2016-01-25