Journal of Comparative Physiology B

, Volume 175, Issue 8, pp 533–541 | Cite as

Physiological mechanisms of thermoregulation in reptiles: a review

Review

Abstract

The thermal dependence of biochemical reaction rates means that many animals regulate their body temperature so that fluctuations in body temperature are small compared to environmental temperature fluctuations. Thermoregulation is a complex process that involves sensing of the environment, and subsequent processing of the environmental information. We suggest that the physiological mechanisms that facilitate thermoregulation transcend phylogenetic boundaries. Reptiles are primarily used as model organisms for ecological and evolutionary research and, unlike in mammals, the physiological basis of many aspects in thermoregulation remains obscure. Here, we review recent research on regulation of body temperature, thermoreception, body temperature set-points, and cardiovascular control of heating and cooling in reptiles. The aim of this review is to place physiological thermoregulation of reptiles in a wider phylogenetic context. Future research on reptilian thermoregulation should focus on the pathways that connect peripheral sensing to central processing which will ultimately lead to the thermoregulatory response.

Keywords

Body temperature Evolution Thermoreception Endothermy Ectothermy Metabolism Control Heat Cardiovascular 

Abbreviations

TRP

Transient receptor potential

NO

Nitric oxide

NOS

Nitric oxide synthase

COX

Cyclooxygenase enzyme

CPT

8-Cyclopentyltheophylline

References

  1. Altimiras J, Franklin CE, Axelsson M (1998) Relationship between blood pressure and heart rate in the salt water crocodile Crocodylus porosus. J Exp Biol 201:2235–2242PubMedGoogle Scholar
  2. Axelrod J (1974) The pineal gland: a neurochemical transducer. Science 184:1341–1348PubMedCrossRefGoogle Scholar
  3. Barros RCH, Branco LGS (1999) Role of central adenosine in the respiratory and thermoregulatory responses to hypoxia. Neuroreport 11:193–197CrossRefGoogle Scholar
  4. Bartholomew GA, Tucker VA (1963) Control of changes in body temperature, metabolism, and circulation by the agamid lizard, Amphibolurus barbatus. Physiol Zool 36:199–218Google Scholar
  5. Bernheim HA, Kluger MJ (1976) Fever and antipyresis in the lizard Dipsosaurus dorsalis. Am J Physiol 231:198–203PubMedGoogle Scholar
  6. Bicego KC, Branco LGS (2002) Discrete electrolytic lesion of the preoptic area prevents LPS-induced behavioral fever in toads. J Exp Biol 205:3513–3518PubMedGoogle Scholar
  7. Bicego KC, Steiner AA, Antunes-Rodrigues J, Branco LGS (2002) Indomethacin impairs LPS-induced behavioral fever in toads. J Appl Physiol 93:512–516PubMedGoogle Scholar
  8. Boyen BD, Sylvia VL, Dean DD, Schwartz Z (2002) Membrane mediated signalling mechanisms are used differentially by metabolites of vitamin D3 in musculoskeletal cells. Steroids 67:421–427CrossRefPubMedGoogle Scholar
  9. Brand MD, Couture P, Else PL, Withers KW, Hulbert AJ (1991) Evolution of energy metabolism. Biochem J 275:81–86PubMedGoogle Scholar
  10. Brand MD, Couture P, Hulbert AJ (1994) Liposomes from mammalian liver mitochondria are more polyunsaturated and leakier to protons than those from reptiles. Comp Biochem Physiol 108B:181–188CrossRefGoogle Scholar
  11. Brand MD, Affouttit C, Esteves TC, Green K, Lambert AJ, Miwa S, Pakay JL, Parker N (2004) Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Rad Biol Med 37:755–767CrossRefPubMedGoogle Scholar
  12. Brown BR (2003) Sensing temperature without ion channels. Nature 421:494–495Google Scholar
  13. Brüning G, Wiese S, Mayer B (1994) Nitric oxide synthase in the brain of the turtle Pseudemys scripta elegans. J Comp Neurol 348:183–206CrossRefPubMedGoogle Scholar
  14. Caterina MJ, Schumacher MA, Tominaga M, Rosen T, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816–824CrossRefPubMedGoogle Scholar
  15. Cesare P, McNaughton P (1996) A novel heat-activated current in nociceptive neurons and its sensitization by bradykinin. Proc Natl Acad Sci USA 93:15435–15439CrossRefPubMedGoogle Scholar
  16. de Cock Buning T (1983) Thermal sensitivity as a specialization for prey capture and feeding in snakes. Amer Zool 23:363–375Google Scholar
  17. Cooper KE (2002) Molecular biology of thermoregulation. Some historical perspectives on thermoregulation. J Appl Physiol 92:1717–1724PubMedGoogle Scholar
  18. Cothran ML, Hutchison VH (1979) Effects of melatonin on thermal selection by Crotaphytus collaris (Squamata: Iguanidae). Comp Biochem Physiol A 63:461–466CrossRefGoogle Scholar
  19. Cowles RB, Bogert CM (1944) A preliminary study of the thermal requirements of desert reptiles. Bull Am Mus Nat Hist 83:261–296Google Scholar
  20. DiBona GF (2003) Thermoregulation. Am J Physiol 284(2):R277–R279Google Scholar
  21. Dzialowski EM, O’Connor MP (2001) Physiological control of warming and cooling during simulated shuttling and basking in lizards. Physiol Biochem Zool 74:679–693CrossRefPubMedGoogle Scholar
  22. Dzialowski EM, O’Connor MP (2004) Importance of the limbs in the physiological control of heat exchange in Iguana iguana and Sceloporus undulatus. J Therm Biol 29:299–305CrossRefGoogle Scholar
  23. Else PL, Hulbert AJ (1981) Comparisons of the “mammal machine” and the “reptile machine”: energy production. Am J Physiol 240:R3–R9PubMedGoogle Scholar
  24. Else PL, Hulbert AJ (1985) An allometric comparison of the mitochondria of mammalian and reptilian tissues: the implications for the evolution of endothermy. J Comp Physiol 156:3–11Google Scholar
  25. Else PL, Hulbert AJ (2003) Membranes as metabolic pacemakers. Clin Exp Parmacol Physiol 30:559–564CrossRefGoogle Scholar
  26. Erskine DJ, Hutchison VH (1981) Melatonin and behavioral thermoregulation in the turtle, Terrapene carolina triunguis. Physiol Behav 26:991–994CrossRefPubMedGoogle Scholar
  27. Ewert MA, Nelson CE (2003) Metabolic heating of embryos and sex determination in the American alligator, alligator mississippiensis. J Therm Biol 28:159–165CrossRefGoogle Scholar
  28. Feldberg W, Saxena PN (1971) Further studies on prostaglandin E 1 fever in cats. J Physiol 219:739–745PubMedGoogle Scholar
  29. Ferguson GW, Gehrmann WH, Karsten KB, Hammack SH, McRae M, Chen TC, Lung NP, Holick MF (2003) Do panther chameleons bask to regulate endogenous vitamin D3 production? Physiol Biochem Zool 76:52–59CrossRefPubMedGoogle Scholar
  30. Ferguson GW, Gehrmann WH, Karsten KB, Landwer AJ, Carman EN, Chen TC, Holick MF (2005) Ultraviolet exposure and vitamin D synthesis in a sun-dwelling and a shade-dwelling species of anolis: are there adaptations for lower ultraviolet B and dietary vitamin D-3 availability in the shade? Physiol Biochem Zool 78:193–200CrossRefPubMedGoogle Scholar
  31. Franklin CE, Seebacher F (2003) The effect of heat transfer mode on heart rate responses and hysteresis during heating and cooling in the estuarine crocodile Crocodylus porosus. J Exp Biol 206:1143–1151CrossRefPubMedGoogle Scholar
  32. Goudkamp JE, Seebacher F, Ahern M, Franklin CE (2004) Physiological thermoregulation in a crustacean? Heart rate hysteresis in the freshwater crayfish Cherax destructor. Comp Biochem Physiol A 138:399–403Google Scholar
  33. Grigg GC, Alchin J (1976) The role of the cardiovascular system in thermoregulation of Crocodylus johnstoni. Physiol Zool 49:24–36Google Scholar
  34. Grigg GC, Drane CR, Courtice GP (1979) Time constants of heating and cooling in the eastern water dragon, Physignathus lesueruii, and some generalizations about heating and cooling in reptiles. J Therm Biol 4:95–103CrossRefGoogle Scholar
  35. Grigg GC, Seebacher F (1999) Field test of a paradigm: hysteresis of heart rate in thermoregulation by a free-ranging lizard (Pogona barbata). Proc Roy Soc Lond B 266:1291–1297CrossRefGoogle Scholar
  36. Guderley H (2004) Metabolic responses to low temperature in fish muscle. Biol Rev 79:409–427CrossRefPubMedGoogle Scholar
  37. Guderley H, St. Pierre J (2002) Going with the flow or life in the fast lane: contrasting mitochondrial responses to thermal change. J Exp Biol 205:2237–2249PubMedGoogle Scholar
  38. Gvozdik L (2002) To heat or to save time? Thermoregulation in the lizard Zootoca vivipara (Squamata: lacertidae) in different thermal environments along an altitudinal gradient. Can J Zool 80:479–492CrossRefGoogle Scholar
  39. Hertz PE (1992) Temperature regulation in Puerto Rican Anolis lizards: a field test using null hypotheses. Ecology 73:1405–1417CrossRefGoogle Scholar
  40. Hertz PE, Huey RB, Stevenson RD (1993) Evaluating temperature regulation by field-active ectotherms: the fallacy of the inappropriate question. Am Nat 142:796–818CrossRefPubMedGoogle Scholar
  41. Hulbert AJ, Else PL (1999) Membranes as possible pacemakers of metabolism. J Theor Biol 199:257–274CrossRefPubMedGoogle Scholar
  42. Johnston IA, Temple GK (2002) Thermal plasticity of skeletal muscle phenotype in ectothermic vertebrates and its significance for locomotory behaviour. J Exp Biol 205:2305–2322PubMedGoogle Scholar
  43. Jones BS, Lynn WF, Stone MO (2001) Thermal modeling of snake infrared reception: evidence for limited detection range. J Theor Biol 209:201–211CrossRefPubMedGoogle Scholar
  44. Kabat AP, Rose RW, West AK (2004) Molecular identification of uncoupling proteins 2 and 3 in a carnivorous marsupial, the Tasmanian devil (Sarcophilus harrisii). Physiol Biochem Zool 77:109–115CrossRefPubMedGoogle Scholar
  45. Kadenbach B (2003) Intrinsic and extrinsic uncoupling of oxidative phosphorylation. Biochim Biophys Acta 1604:77–94PubMedCrossRefGoogle Scholar
  46. Kauffman A, Cabrera A, Zucker I (2001) Energy intake and fur in summer- and winter-acclimated Siberian hamsters (Phodopus sungorus). Am J Physiol 281:R519–R527Google Scholar
  47. Krochmal AR, Bakken GS (2003) Thermoregulation is the pits: use of thermal radiation for retreat site selection by rattlesnakes. J Exp Biol 206:2539–2545CrossRefPubMedGoogle Scholar
  48. Krochmal AR, Bakken GS, LaDuc TJ (2004) Heat in evolution’s kitchen: evolutionary perspectives on the functions and origin of the facial pit of pitvipers (Viperidae: Crotalinae). J Exp Biol 207:4231–4238CrossRefPubMedGoogle Scholar
  49. Krotewicz M, Lewinski A (1994) Thyroid hormone secretion in male Wistar rats treated with melatonin and/or thyrotropin; dependence of effects on the used doses. Neuroendocrin Lett 16:263–268Google Scholar
  50. Kvadsheim PH, Aarseth JJ (2002) Thermal function of phocid seal fur. Mar Mamm Sci 18:952–962CrossRefGoogle Scholar
  51. Lutterschmidt DI, Lutterschmidt WI, Hutchison VH (1997) Melatonin and chlorpromazine: thermal selection and metabolic rate in the bullsnake, Pituophis melanoleucus. Comp Biochem Physiol C 118:271–277CrossRefGoogle Scholar
  52. Lutterschmidt DI, Lutterschmidt WI, Ford NB, Hutchison VH (2002) Behavioral thermoregulation and the role of melatonin in a nocturnal snake. Horm Behav 41:41–50CrossRefPubMedGoogle Scholar
  53. Madden CJ, Morrison SF (2004) Excitatory amino acid receptors in the dorsomedial hypothalamus mediate prostaglandin-evoked thermogenesis in brown adipose tissue. Am J Physiol 286:R320–R325Google Scholar
  54. Mathai ML, Arnold I, Febbraio MA, McKinley MJ (2004) Central blockade of nitric oxide induces hyperthermia that is prevented by indomethacin in rats. J Therm Biol 29:401–405CrossRefGoogle Scholar
  55. Mendoça MT, Tousignant AJ, Crews D (1995) Seasonal changes and annual variability in daily plasma melatonin in the red-sided garter snake (Thamnophis sirtalis parietalis). Gen Comp Endocrinol 100:226–237CrossRefPubMedGoogle Scholar
  56. Moiseenkova V, Bell B, Motamedi M, Wozniak E, Christensen B (2003) Am J Physiol 284:R598–R606Google Scholar
  57. Moon C (2004) An investigation of the effects of ruthenium red, nitric oxide and endothelin-1 on infrared receptor activity in a crotaline snake. Neuroscience 124:913–918CrossRefPubMedGoogle Scholar
  58. Moon C, Terashima S, Shin T (2003) Immunohistochemical localization of the delta subspecies of protein kinase C in the trigeminal sensory system of Trimeresurus flavoviridis, an infrared sensitive snake. Neurosci Lett 338:233–236CrossRefPubMedGoogle Scholar
  59. Morgareidge KR, White FN (1972) Cutaneous vascular changes during heating and cooling in the Galapagos marine iguana. Nature 223:587–591CrossRefGoogle Scholar
  60. O’Connor MP (1999) Physiological and ecological implications of a simple model of heating and cooling in reptiles. J Therm Biol 24:113–136CrossRefGoogle Scholar
  61. Patapoutian A, Peier AM, Story GM, Viswanath V (2003) ThermoTRP channels and beyond: mechanisms of temperature sensation. Nature Rev Neurosci 4:529–539CrossRefGoogle Scholar
  62. Petersen AM, Gleeson TT, Scholnick DA (2003) The effect of oxygen and adenosine on lizard thermoregulation. Physiol Biochem Zool 76:339–347CrossRefPubMedGoogle Scholar
  63. Raimbault S, Dridi S, Denjean F, Lachuer J, Couplan E, Bouillaud F, Bordas A, Duchamp C, Taouis M, Ricquier D (2001) An uncoupling protein homologue putatively involved in facultative muscle thermogenesis in birds. Biochem J 353:441–444CrossRefPubMedGoogle Scholar
  64. Romanovsky AA, Ivanov AI, Shimansky YP (2002) Ambient temperature for experiments in rats: a new method for determining the zone of thermal neutrality. J Appl Physiol 92:2667–2679PubMedGoogle Scholar
  65. Sakamoto K, Liu C, Tosini G (2004) Circadian rhythms in the retina of rats with photoreceptor degeneration. J Neurochem 90:1019–1024CrossRefPubMedGoogle Scholar
  66. Salvemini D (1997) Regulation of cyclooxygenase enzymes by nitric oxide. Cell Mol Life Sci 53:576–582PubMedCrossRefGoogle Scholar
  67. Seebacher F (1999) Behavioural postures and the rate of body temperature change in wild freshwater crocodiles, Crocodylus johnstoni. Physiol Biochem Zool 72:57–63CrossRefPubMedGoogle Scholar
  68. Seebacher F (2000) Heat transfer in a microvascular network: the effect of heart rate on heating and cooling in reptiles (Pogona barbata and Varanus varius). J Theor Biol 203:97–109CrossRefPubMedGoogle Scholar
  69. Seebacher F, Franklin CE (2001) Control of heart rate during thermoregulation in the heliothermic lizard, Pogona barbata: importance of cholinergic and adrenergic mechanisms. J Exp Biol 204:4361–4366PubMedGoogle Scholar
  70. Seebacher F, Franklin CE (2003) Prostaglandins are important in thermoregulation of a lizard (Pogona vitticeps). Proc Roy Soc Lond B (Suppl) 270:S50–S53CrossRefGoogle Scholar
  71. Seebacher F, Franklin CE (2004a) Integration of autonomic and local mechanisms in regulating cardiovascular responses to heating and cooling in a reptile (Crocodylus porosus). J Comp Physiol B 174:577–585CrossRefPubMedGoogle Scholar
  72. Seebacher F, Franklin CE (2004b) Cardiovascular mechanisms during thermoregulation in reptiles. Int Congr Ser 1275:242–249CrossRefGoogle Scholar
  73. Seebacher F, Grigg GC (2001) Changes in heart rate are important for thermoregulation in the varanid lizard, Varanus varius. J Comp Physiol B 171:395–400CrossRefPubMedGoogle Scholar
  74. Seebacher F, Shine R (2004) Evaluating thermoregulation in reptiles: the fallacy of the inappropriately applied method. Physiol Biochem Zool 77:688–695CrossRefPubMedGoogle Scholar
  75. Seebacher F, Grigg GC, Beard LA (1999) Crocodiles as dinosaurs: behavioural thermoregulation in very large ectotherms leads to high and stable body temperatures. J Exp Biol 202:77–86PubMedGoogle Scholar
  76. Seebacher F, Elsey RM, Trosclair PL III (2003) Body temperature null-distributions in large reptiles: seasonal thermoregulation in the American alligator (Alligator mississippiensis). Physiol Biochem Zool 76:348–359CrossRefPubMedGoogle Scholar
  77. Shine R, Sun L (2002) Arboreal ambush site selection by pit-vipers Gloydius shedaoensis. Anim Behav 63:565–576CrossRefGoogle Scholar
  78. Sievert LM, Poore JL (1995) Melatonin does not influence thermoregulatory behavior in Bufo americanus and Bufo marinus. Copeia 1995:490–494CrossRefGoogle Scholar
  79. Smeets WJ, Alonso JR, Gonzalez A (1997) Distribution of NADPH-diaphorase and nitric oxide synthase in relation to catecholaminergic neuronal structures in the brain of the lizard Gekko gecko. J Comp Neurol 377:121–141CrossRefPubMedGoogle Scholar
  80. Soares D (2002) An ancient sensory organ in crocodilians. Nature 417:241–242CrossRefPubMedGoogle Scholar
  81. Steiner AA, Branco LSG (2002) Hypoxia-induced anapyrexia: implications and putative mediators. Annu Rev Physiol 64:263–288CrossRefPubMedGoogle Scholar
  82. Tosini G, Menaker M (1996) The pineal complex and melatonin affect the expression of the daily rhythm of behavioral thermoregulation in the green iguana. J Comp Physiol A 179:135–142CrossRefPubMedGoogle Scholar
  83. Tosini G, Bertolucci C, Foà A (2001) The circadian system of reptiles: a multioscillatory and multiphotoreceptive system. Physiol Behav 72:461–471CrossRefPubMedGoogle Scholar
  84. Turner N, Else PL, Hulbert AJ (2003) Docosahexaenoic acid (DHA) content of membranes determines molecular activity of the sodium pump: implications for disease and metabolism. Naturwiss 90:521–523CrossRefPubMedGoogle Scholar
  85. Viana F, de la Pena E, Belmonte C (2002) Specificity of cold thermotransduction is determined by differential ionic channel expression. Nat Neurosci 5:254–260CrossRefPubMedGoogle Scholar
  86. Viswanath V, Story GM, Peier AM, Petrus MJ, Lee VM, Hwang SW, Patapoutian A, Jegla T (2003) Opposite thermosensor in fruitfly and mouse. Nature 423:822–823CrossRefPubMedGoogle Scholar
  87. Wagner EL, Gleeson TT (1997) Postexercise thermoregulatory behavior and recovery from exercise in desert iguanas. Physiol Behav 61:175–180CrossRefPubMedGoogle Scholar
  88. Woodbury CJ, Zwick M, Wang S, Lawson JJ, Caterina MJ, Koltzenburg M, Albers KM, Koerber HR, Davis BM (2004) Nociceptors lacking TRPV1 and TRPV2 have normal heat responses. J Neurosci 24:6410–6415CrossRefPubMedGoogle Scholar
  89. Woods HA, Harrison JF (2002) Interpreting rejections of the beneficial acclimation hypothesis: when is physiological plasticity adaptive? Evolution 56:1863–1866PubMedGoogle Scholar
  90. Wright ML, Pikula A, Cykowski LJ, Kuliga K (1996) Effect of melatonin on the anuran thyroid gland: follicle cell proliferation, morphometry, and subsequent thyroid hormone secretion in vivo after melatonin treatment in vivo. Gen Comp Endocrinol 103:182–191CrossRefPubMedGoogle Scholar
  91. Wu BJ, Hulbert AJ, Storlien LH, Else PL (2004) Membrane lipids and sodium pumps of cattle and crocodiles: an experimental test of the membrane pacemaker theory of metabolism. Am J Physiol 287:R633–R641CrossRefGoogle Scholar
  92. Zaar M, Larsen E, Wang T (2004) Hysteresis of heart rate and heat exchange of fasting and postprandial savannah monitor lizards (Varanus exanthematicus). Comp Biochem Physiol 137A:675–682CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Integrative Physiology, School of Biological Sciences A08University of SydneySydneyAustralia
  2. 2.School of Integrative BiologyThe University of QueenslandSt. LuciaAustralia

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