Abstract
Thermoregulation is of great importance for the survival and fitness of ectotherms as physiological functions are optimized within a narrow range of body temperature (T b). The precision with which reptiles thermoregulate has been proposed to be related to the thermal quality of their environments. Although a number of studies have looked at the effect of thermal constraints imposed by diel, seasonal and altitudinal variation on thermoregulatory strategies, few have addressed this question in a laboratory setting. We conducted a laboratory experiment to test whether tuatara, Sphenodon punctatus (order Rhynchocephalia), a cold-adapted reptile endemic to New Zealand, modify their thermoregulatory behaviour in response to different thermal environments. We provided tuatara with three thermal treatments: high-quality habitat [preferred T b (T sel) could be reached for 8 h/day], medium-quality habitat (T sel available for 5 h/day) and low-quality habitat (T sel available for 3 h/day). All groups maintained body mass, but tuatara in the low-quality habitat thermoregulated more accurately and tended to maintain higher T bs than tuatara in the high-quality habitat. This study thus provides experimental evidence that reptiles are capable of adjusting their thermoregulatory behaviour in response to different thermal constraints. This result also has implications for the conservation of tuatara. A proposed translocation from their current habitat to a higher latitudinal range within New Zealand (similar to the shift from our 8 h/day to our 5 h/day regime) is unlikely to induce thermoconformity; rather, tuatara will probably engage in more effective thermoregulatory behaviour.
Similar content being viewed by others
References
Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, Oxford
Angilletta MJ, Niewiarowski PH, Navas CA (2002) The evolution of thermal physiology in ectotherms. J Therm Biol 27:249–268
Autumn C, De Nardo DF (1995) Behavioural thermoregulation increases growth rate in a nocturnal lizard. J Herpetol 29:157–162
Avery RA, Bedford JD, Newcombe CP (1982) The role of thermoregulation in lizard biology: predatory efficiency in a temperate diurnal basker. Behav Ecol Sociobiol 11:261–267
Barwick RE (1982) In: Newman DG (ed) Observations on active thermoregulation in the tuatara, Sphenodon punctatus (Reptilia: Rhynchocephalia). New Zealand Wildlife Service Occasional Publication, Wellington, pp 225–236
Bauwens D, Hertz PE, Castilla AM (1996) Thermoregulation in a lacertid lizard: the relative contributions of distinct behavioral mechanisms. Ecology 77:1818–1830
Birchard GF, Nelson NJ, Daugherty CH (2006) A circadian rhythm in oxygen consumption rate in juvenile tuatara (Sphenodon punctatus). New Zeal J Zool 33:185–188
Blouin-Demers G, Nadeau P (2005) The cost-benefit model of thermoregulation does not predict lizard thermoregulatory behavior. Ecology 86:560–566
Blouin-Demers G, Weatherhead PJ (2001) Thermal ecology of black rat snakes (Elaphe obseleta) in a thermally challenging environment. Ecology 82:3025–3043
Brown GP, Weatherhead PJ (2000) Thermal ecology and sexual dimorphism in northern water snakes, Nerodia sipedon. Ecol Monogr 70:311–330
Cadena V, Tattersall GJ (2009) The effect of thermal quality on the thermoregulatory behaviour of the bearded dragon Pogona vitticeps: influences of methodological assessment. Phys Biochem Zool 82:203–217
Cartland LK, Grimmond NM (1994) The effect of temperature on the metabolism of juvenile tuatara, Sphenodon punctatus. New Zeal J Zool 21:373–378
Christian KA, Bedford GS (1995) Seasonal changes in thermoregulation by the frillneck lizard, Chlamydosaurus kingii, in tropical Australia. Ecology 76:124–132
Christian KA, Weavers BW (1996) Thermoregulation of monitor lizards in Australia: an evaluation of methods in thermal biology. Ecol Monogr 66:139–157
Cree A (1994) Low reproductive output in female reptiles from New Zealand. N Z J Zool 21:351–372
Cree A, Butler D (1993) Tuatara recovery plan (Sphenodon spp.). Threatened Species Recovery Plan Series No. 9, New Zealand Department of Conservation, Wellington
Crews D, Bull JJ (2008) Some like it hot, some don’t. Nature 451:527–528
Dubois Y, Blouin-Demers G, Shipley B, Thomas D (2009) Thermoregulation and habitat selection in wood turtles Glyptemys insculpta: chasing the sun slowly. J Anim Ecol 78:1023–1032
Dzialowski EM (2005) Use of operative temperature and standard operative temperature models in thermal biology. J Therm Biol 30:317–334
Edwards AL, Blouin-Demers G (2007) Thermoregulation as a function of thermal quality in a northern population of painted turtles, Chrysemys picta. Can J Zool 85:526–535
Gaze P (2001) Tuatara recovery plan (Sphenodon spp.) 2001–2011. Threatened Species Recovery Plan Series No. 47. New Zealand Department of Conservation, Wellington
Gillingham JC, Carmichael C, Miller T (1995) Social behaviour of the tuatara, Sphenodon punctatus. Herpetol Monogr 9:5–16
Grbac I, Bauwens D (2001) Constraints on temperature regulation in two sympatric Podarcis lizards during autumn. Copeia 2001:178–186
Gvoždík L (2002) To heat or save time? Thermoregulation in the lizard Zootoca vivipara (Squamata: Lacertidae) in different thermal environments along an altitudinal gradient. Can J Zool 80:479–492
Hare JR, Whitworth E, Cree A (2007) Correct orientation of a hand-held infrared thermometer is important for accurate measurement of body temperatures in small lizards and tuatara. Herp Rev 38:311–315
Hay JM, Subramanian S, Millar CD, Mohandesan E, Lambert DM (2008) Rapid molecular evolution in a living fossil. Trends Genet 24:106–109
Herczeg G, Kovacs T, Hettyey A, Merila J (2003) To thermoconform or thermoregulate? An assessment of thermoregulation opportunities for a lizard Zootoca vivipara in the subarctic. Polar Biol 26:486–490
Herczeg G, Gonda A, Saarikivi J, Merila J (2006) Experimental support for the cost-benefit model of lizard thermoregulation. Behav Ecol Sociobiol 60:405–414
Herczeg G, Herrero A, Saarikivi J, Gonda A, Janti M, Merila J (2008) Experimental support for the cost-benefit model of lizard thermoregulation: the effects of predation risk and food supply. Oecologia 155:1–10
Herrel A, James RS, Van Damme R (2007) Fight versus flight: physiological basis for temperature-dependent behavioral shifts in lizards. J Exp Biol 210:1762–1767
Hertz PE, Huey RB, Stevenson RD (1993) Evaluating temperature regulation by field-active ectotherms: the fallacy of the inappropriate question. Am Nat 142:796–818
Hill L (1982) Water relations and excretion of the tuatara, Sphenodon punctatus: an overview. In: Newman DG (ed) Proceedings of a symposium held at Victoria University of Wellington, January 1980, New Zealand Wildlife Service Occasional Publication, Wellington, pp 183–203
Huey RB (1974) Behavioural thermoregulation in lizards: importance of associated costs. Science 31:1001–1003
Huey RB (1982) Temperature, physiology, and the ecology of reptiles. In: Gans C, Pough FH (eds) Biology of the Reptilia, vol 12. Academic Press, New York, pp 25–74
Huey RB, Slatkin M (1976) Costs and benefits of lizard thermoregulation. Q Rev Biol 51:363–384
Mitchell NJ, Kearney MR, Nelson NJ, Porter WP (2008) Predicting the fate of a living fossil: how will global warming affect sex determination and hatching phenology in tuatara? Proc Biol Sci 275:2185–2193
Mondal S, Rai U (2001) In vitro effect of temperature on phagocytic and cytotoxic activities of splenic phagocytes of the wall lizard, Hemidactylus flaviviridis. Comp Biochem Phys A 129:391–398
Row JR, Blouin-Demers G (2006) Thermal quality influences effectiveness of thermoregulation, habitat use, and behaviour in milk snakes. Oecologia 148:1–11
Saint Girons H (1980) Thermoregulation in reptile with special reference to the tuatara and its ecophysiology. Tuatara 24:59–80
Saint Girons H, Bell BD, Newman DG (1980) Observations on the activity and thermoregulation of the tuatara, Sphenodon punctatus (Reptilia: Rhynchocephalia), on Stephens Island. N Z J Zool 7:551–556
Scheers H, Van Damme R (2002) Micro-scale differences in thermal habitat quality and a possible case of evolutionary flexibility in the thermal physiology of lacertid lizard. Oecologia 132:323–331
Shine R, Li-Xin S, Fitzgerald M (2002) Thermal correlates of foraging-site selection by Chinese pit-vipers (Gloydius shedaoensis, Viperidae). J Therm Biol 27:405–412
Statsoft (2003) STATISTICA (data analysis software system), version 6. Available at: http://www.statsoft.com
Terezow MG, Nelson NJ, Markwell TJ (2008) Circadian emergence and movement of captive juvenile tuatara (Sphenodon spp.). N Z J Zool 35:205–216
Towns DR, Daugherty CH (1994) Patterns of range contractions and extinctions in the New Zealand herpetofauna following human colonisation. N Z J Zool 21:325–339
Walls GY (1981) Feeding ecology of the tuatara Sphenodon punctatus on Stephens Island, Cook Strait. N Z J Ecol 4:89–97
Walls GY (1983) Activity of the tuatara and its relationship to weather conditions on Stephens Island, Cook Strait, with observations on geckos and invertebrates. N Z J Zool 10:309–318
Wells RMG, Tetens V, Housley GD, Young AA, Dawson NJ, Johansen K (1990) Effect of temperature on control of breathing in the cryophilic Rhynchocephalian reptile, Sphenodon punctatus. Comp Biochem Phys A 96:33–340
Werner YL, Whitaker AH (1978) Observations and comments on the body temperatures of some New Zealand reptiles. N Z J Zool 5:375–393
Withers PC, Campbell JD (1985) Effects of environmental cost on thermoregulation in the desert iguana. Physiol Zool 58:329–339
Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, London
Acknowledgements
For providing the necessary permits and approvals, we are grateful to the Department of Conservation (permits NELCO-12497) and the University of Otago Animal Ethics Committee (AEC permit 14/06). For consultation, we thank Ngati Koata (kaitiaki or guardians of tuatara from Stephens Island/Takapourewa) and Ngai Tahu (mana whenua of Otago). We thank I. Dickson, C. Allen and J. DeVries and the University of Otago technical staff for assistance in the field and laboratory. For access to animals and/or sites, we thank Peacock Springs Conservation Park, Orokonui Ecosanctuary, Karori Wildlife Sanctuary and Southland Museum and Art Gallery. We also thank the Cree Lab members for valuable comments on early drafts. This work was supported by the Department of Zoology, University of Otago, New Zealand.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Raoul Van Damme.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Besson, A.A., Cree, A. A cold-adapted reptile becomes a more effective thermoregulator in a thermally challenging environment. Oecologia 163, 571–581 (2010). https://doi.org/10.1007/s00442-010-1571-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-010-1571-y