Physiological Mechanisms of Thermoregulation in Reptiles
Physiological Mechanisms of Thermoregulation in Reptiles
Physiological Mechanisms of Thermoregulation in Reptiles
DOI 10.1007/s00360-005-0007-1
R EV IE W
Received: 15 February 2005 / Revised: 29 April 2005 / Accepted: 20 May 2005 / Published online: 27 July 2005
Ó Springer-Verlag 2005
Thermoreception
Future research on reptilian thermoregulation should Brand MD, Affouttit C, Esteves TC, Green K, Lambert AJ, Miwa
focus on the pathways that connect peripheral sensing to S, Pakay JL, Parker N (2004) Mitochondrial superoxide: pro-
duction, biological effects, and activation of uncoupling pro-
central processing which will ultimately lead to the ther- teins. Free Rad Biol Med 37:755–767
moregulatory response. Sensing of the thermal environ- Brown BR (2003) Sensing temperature without ion channels.
ment is particularly important for behavioural Nature 421:494–495
thermoregulation, and although the pineal complex and Brüning G, Wiese S, Mayer B (1994) Nitric oxide synthase in the
brain of the turtle Pseudemys scripta elegans. J Comp Neurol
melatonin provide a mechanism to process environmen- 348:183–206
tal conditions, it seems likely that there also exist other, Caterina MJ, Schumacher MA, Tominaga M, Rosen T, Levine JD,
peripheral sensors. For example, restricted local heating Julius D (1997) The capsaicin receptor: a heat-activated ion
of a dorsal section in a crocodile and a lizard elicited a channel in the pain pathway. Nature 389:816–824
distinct cardiovascular response (Morgareidge and White Cesare P, McNaughton P (1996) A novel heat-activated current in
nociceptive neurons and its sensitization by bradykinin. Proc
1972; Grigg and Alchin 1976) that must have been inde- Natl Acad Sci USA 93:15435–15439
pendent from direct stimulation of the pineal. Rather, we de Cock Buning T (1983) Thermal sensitivity as a specialization for
speculate that peripheral thermal sensors are present in prey capture and feeding in snakes. Amer Zool 23:363–375
reptiles, and these sensors may be similar to the inner- Cooper KE (2002) Molecular biology of thermoregulation. Some
historical perspectives on thermoregulation. J Appl Physiol
vated thermal sensor proteins found in mammals and 92:1717–1724
Drosophila (Patapoutian et al. 2003). Central processing Cothran ML, Hutchison VH (1979) Effects of melatonin on ther-
of the peripheral thermal information may involve the mal selection by Crotaphytus collaris (Squamata: Iguanidae).
NOS–NO–COX axis that could integrate set-points and Comp Biochem Physiol A 63:461–466
Cowles RB, Bogert CM (1944) A preliminary study of the thermal
cardiovascular control. It is of particular interest that the requirements of desert reptiles. Bull Am Mus Nat Hist 83:261–
cardiovascular response to heating and cooling in reptiles 296
is at least in part mediated by the integration between the DiBona GF (2003) Thermoregulation. Am J Physiol 284(2):R277–
baroreflex and systemically acting NOS and COX en- R279
zymes (Altimiras et al. 1998; Seebacher and Franklin Dzialowski EM, O’Connor MP (2001) Physiological control of
warming and cooling during simulated shuttling and basking in
2003; Seebacher and Franklin 2004a). A link between the lizards. Physiol Biochem Zool 74:679–693
local and central functions of COX and NO may connect Dzialowski EM, O’Connor MP (2004) Importance of the limbs in
environmental stimuli to the heart rate hysteresis that is the physiological control of heat exchange in Iguana iguana and
typical of reptilian thermoregulation. Sceloporus undulatus. J Therm Biol 29:299–305
Else PL, Hulbert AJ (1981) Comparisons of the ‘‘mammal ma-
chine’’ and the ‘‘reptile machine’’: energy production. Am J
Acknowledgments This work was supported by an Australian Re- Physiol 240:R3–R9
search Council Discovery grant to F.S. and C.E.F. 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
156:3–11
References Else PL, Hulbert AJ (2003) Membranes as metabolic pacemakers.
Clin Exp Parmacol Physiol 30:559–564
Altimiras J, Franklin CE, Axelsson M (1998) Relationship between Erskine DJ, Hutchison VH (1981) Melatonin and behavioral
blood pressure and heart rate in the salt water crocodile Croc- thermoregulation in the turtle, Terrapene carolina triunguis.
odylus porosus. J Exp Biol 201:2235–2242 Physiol Behav 26:991–994
Axelrod J (1974) The pineal gland: a neurochemical transducer. Ewert MA, Nelson CE (2003) Metabolic heating of embryos and
Science 184:1341–1348 sex determination in the American alligator, alligator missis-
Barros RCH, Branco LGS (1999) Role of central adenosine in the sippiensis. J Therm Biol 28:159–165
respiratory and thermoregulatory responses to hypoxia. Neu- Feldberg W, Saxena PN (1971) Further studies on prostaglandin E
roreport 11:193–197 1 fever in cats. J Physiol 219:739–745
Bartholomew GA, Tucker VA (1963) Control of changes in body Ferguson GW, Gehrmann WH, Karsten KB, Hammack SH,
temperature, metabolism, and circulation by the agamid lizard, McRae M, Chen TC, Lung NP, Holick MF (2003) Do panther
Amphibolurus barbatus. Physiol Zool 36:199–218 chameleons bask to regulate endogenous vitamin D3 produc-
Bernheim HA, Kluger MJ (1976) Fever and antipyresis in the lizard tion? Physiol Biochem Zool 76:52–59
Dipsosaurus dorsalis. Am J Physiol 231:198–203 Ferguson GW, Gehrmann WH, Karsten KB, Landwer AJ, Car-
Bicego KC, Branco LGS (2002) Discrete electrolytic lesion of the man EN, Chen TC, Holick MF (2005) Ultraviolet exposure and
preoptic area prevents LPS-induced behavioral fever in toads. J vitamin D synthesis in a sun-dwelling and a shade-dwelling
Exp Biol 205:3513–3518 species of anolis: are there adaptations for lower ultraviolet B
Bicego KC, Steiner AA, Antunes-Rodrigues J, Branco LGS (2002) and dietary vitamin D-3 availability in the shade? Physiol
Indomethacin impairs LPS-induced behavioral fever in toads. J Biochem Zool 78:193–200
Appl Physiol 93:512–516 Franklin CE, Seebacher F (2003) The effect of heat transfer mode
Boyen BD, Sylvia VL, Dean DD, Schwartz Z (2002) Membrane on heart rate responses and hysteresis during heating and
mediated signalling mechanisms are used differentially by cooling in the estuarine crocodile Crocodylus porosus. J Exp
metabolites of vitamin D3 in musculoskeletal cells. Steroids Biol 206:1143–1151
67:421–427 Goudkamp JE, Seebacher F, Ahern M, Franklin CE (2004)
Brand MD, Couture P, Else PL, Withers KW, Hulbert AJ (1991) Physiological thermoregulation in a crustacean? Heart rate
Evolution of energy metabolism. Biochem J 275:81–86 hysteresis in the freshwater crayfish Cherax destructor. Comp
Brand MD, Couture P, Hulbert AJ (1994) Liposomes from mam- Biochem Physiol A 138:399–403
malian liver mitochondria are more polyunsaturated and leak- Grigg GC, Alchin J (1976) The role of the cardiovascular system
ier to protons than those from reptiles. Comp Biochem Physiol in thermoregulation of Crocodylus johnstoni. Physiol Zool
108B:181–188 49:24–36
540
Grigg GC, Drane CR, Courtice GP (1979) Time constants of Moon C (2004) An investigation of the effects of ruthenium red,
heating and cooling in the eastern water dragon, Physignathus nitric oxide and endothelin-1 on infrared receptor activity in a
lesueruii, and some generalizations about heating and cooling in crotaline snake. Neuroscience 124:913–918
reptiles. J Therm Biol 4:95–103 Moon C, Terashima S, Shin T (2003) Immunohistochemical
Grigg GC, Seebacher F (1999) Field test of a paradigm: hysteresis localization of the delta subspecies of protein kinase C in the
of heart rate in thermoregulation by a free-ranging lizard trigeminal sensory system of Trimeresurus flavoviridis, an
(Pogona barbata). Proc Roy Soc Lond B 266:1291–1297 infrared sensitive snake. Neurosci Lett 338:233–236
Guderley H (2004) Metabolic responses to low temperature in fish Morgareidge KR, White FN (1972) Cutaneous vascular changes
muscle. Biol Rev 79:409–427 during heating and cooling in the Galapagos marine iguana.
Guderley H, St. Pierre J (2002) Going with the flow or life in the Nature 223:587–591
fast lane: contrasting mitochondrial responses to thermal O’Connor MP (1999) Physiological and ecological implications of a
change. J Exp Biol 205:2237–2249 simple model of heating and cooling in reptiles. J Therm Biol
Gvozdik L (2002) To heat or to save time? Thermoregulation in the 24:113–136
lizard Zootoca vivipara (Squamata: lacertidae) in different Patapoutian A, Peier AM, Story GM, Viswanath V (2003) Ther-
thermal environments along an altitudinal gradient. Can J Zool moTRP channels and beyond: mechanisms of temperature
80:479–492 sensation. Nature Rev Neurosci 4:529–539
Hertz PE (1992) Temperature regulation in Puerto Rican Petersen AM, Gleeson TT, Scholnick DA (2003) The effect of
Anolis lizards: a field test using null hypotheses. Ecology oxygen and adenosine on lizard thermoregulation. Physiol
73:1405–1417 Biochem Zool 76:339–347
Hertz PE, Huey RB, Stevenson RD (1993) Evaluating temperature Raimbault S, Dridi S, Denjean F, Lachuer J, Couplan E, Bouillaud
regulation by field-active ectotherms: the fallacy of the inap- F, Bordas A, Duchamp C, Taouis M, Ricquier D (2001) An
propriate question. Am Nat 142:796–818 uncoupling protein homologue putatively involved in faculta-
Hulbert AJ, Else PL (1999) Membranes as possible pacemakers of tive muscle thermogenesis in birds. Biochem J 353:441–444
metabolism. J Theor Biol 199:257–274 Romanovsky AA, Ivanov AI, Shimansky YP (2002) Ambient
Johnston IA, Temple GK (2002) Thermal plasticity of skeletal temperature for experiments in rats: a new method for
muscle phenotype in ectothermic vertebrates and its significance determining the zone of thermal neutrality. J Appl Physiol
for locomotory behaviour. J Exp Biol 205:2305–2322 92:2667–2679
Jones BS, Lynn WF, Stone MO (2001) Thermal modeling of snake Sakamoto K, Liu C, Tosini G (2004) Circadian rhythms in the
infrared reception: evidence for limited detection range. J Theor retina of rats with photoreceptor degeneration. J Neurochem
Biol 209:201–211 90:1019–1024
Kabat AP, Rose RW, West AK (2004) Molecular identification of Salvemini D (1997) Regulation of cyclooxygenase enzymes by nitric
uncoupling proteins 2 and 3 in a carnivorous marsupial, the oxide. Cell Mol Life Sci 53:576–582
Tasmanian devil (Sarcophilus harrisii). Physiol Biochem Zool Seebacher F (1999) Behavioural postures and the rate of body
77:109–115 temperature change in wild freshwater crocodiles, Crocodylus
Kadenbach B (2003) Intrinsic and extrinsic uncoupling of oxidative johnstoni. Physiol Biochem Zool 72:57–63
phosphorylation. Biochim Biophys Acta 1604:77–94 Seebacher F (2000) Heat transfer in a microvascular network: the
Kauffman A, Cabrera A, Zucker I (2001) Energy intake and fur in effect of heart rate on heating and cooling in reptiles (Pogona
summer- and winter-acclimated Siberian hamsters (Phodopus barbata and Varanus varius). J Theor Biol 203:97–109
sungorus). Am J Physiol 281:R519–R527 Seebacher F, Franklin CE (2001) Control of heart rate during
Krochmal AR, Bakken GS (2003) Thermoregulation is the pits: use thermoregulation in the heliothermic lizard, Pogona barbata:
of thermal radiation for retreat site selection by rattlesnakes. J importance of cholinergic and adrenergic mechanisms. J Exp
Exp Biol 206:2539–2545 Biol 204:4361–4366
Krochmal AR, Bakken GS, LaDuc TJ (2004) Heat in evolution’s Seebacher F, Franklin CE (2003) Prostaglandins are important in
kitchen: evolutionary perspectives on the functions and origin thermoregulation of a lizard (Pogona vitticeps). Proc Roy Soc
of the facial pit of pitvipers (Viperidae: Crotalinae). J Exp Biol Lond B (Suppl) 270:S50–S53
207:4231–4238 Seebacher F, Franklin CE (2004a) Integration of autonomic and
Krotewicz M, Lewinski A (1994) Thyroid hormone secretion in local mechanisms in regulating cardiovascular responses to
male Wistar rats treated with melatonin and/or thyrotropin; heating and cooling in a reptile (Crocodylus porosus). J Comp
dependence of effects on the used doses. Neuroendocrin Lett Physiol B 174:577–585
16:263–268 Seebacher F, Franklin CE (2004b) Cardiovascular mechanisms
Kvadsheim PH, Aarseth JJ (2002) Thermal function of phocid seal during thermoregulation in reptiles. Int Congr Ser 1275:242–
fur. Mar Mamm Sci 18:952–962 249
Lutterschmidt DI, Lutterschmidt WI, Hutchison VH (1997) Mel- Seebacher F, Grigg GC (2001) Changes in heart rate are important
atonin and chlorpromazine: thermal selection and metabolic for thermoregulation in the varanid lizard, Varanus varius. J
rate in the bullsnake, Pituophis melanoleucus. Comp Biochem Comp Physiol B 171:395–400
Physiol C 118:271–277 Seebacher F, Shine R (2004) Evaluating thermoregulation in rep-
Lutterschmidt DI, Lutterschmidt WI, Ford NB, Hutchison VH tiles: the fallacy of the inappropriately applied method. Physiol
(2002) Behavioral thermoregulation and the role of melatonin Biochem Zool 77:688–695
in a nocturnal snake. Horm Behav 41:41–50 Seebacher F, Grigg GC, Beard LA (1999) Crocodiles as dinosaurs:
Madden CJ, Morrison SF (2004) Excitatory amino acid receptors behavioural thermoregulation in very large ectotherms leads to
in the dorsomedial hypothalamus mediate prostaglandin- high and stable body temperatures. J Exp Biol 202:77–86
evoked thermogenesis in brown adipose tissue. Am J Physiol Seebacher F, Elsey RM, Trosclair PL III (2003) Body temperature
286:R320–R325 null-distributions in large reptiles: seasonal thermoregulation in
Mathai ML, Arnold I, Febbraio MA, McKinley MJ (2004) Central the American alligator (Alligator mississippiensis). Physiol
blockade of nitric oxide induces hyperthermia that is prevented Biochem Zool 76:348–359
by indomethacin in rats. J Therm Biol 29:401–405 Shine R, Sun L (2002) Arboreal ambush site selection by pit-vipers
Mendoça MT, Tousignant AJ, Crews D (1995) Seasonal changes Gloydius shedaoensis. Anim Behav 63:565–576
and annual variability in daily plasma melatonin in the red- Sievert LM, Poore JL (1995) Melatonin does not influence ther-
sided garter snake (Thamnophis sirtalis parietalis). Gen Comp moregulatory behavior in Bufo americanus and Bufo marinus.
Endocrinol 100:226–237 Copeia 1995:490–494
Moiseenkova V, Bell B, Motamedi M, Wozniak E, Christensen B Smeets WJ, Alonso JR, Gonzalez A (1997) Distribution of
(2003) Am J Physiol 284:R598–R606 NADPH-diaphorase and nitric oxide synthase in relation to
541
catecholaminergic neuronal structures in the brain of the lizard Wagner EL, Gleeson TT (1997) Postexercise thermoregulatory
Gekko gecko. J Comp Neurol 377:121–141 behavior and recovery from exercise in desert iguanas. Physiol
Soares D (2002) An ancient sensory organ in crocodilians. Nature Behav 61:175–180
417:241–242 Woodbury CJ, Zwick M, Wang S, Lawson JJ, Caterina MJ, Kol-
Steiner AA, Branco LSG (2002) Hypoxia-induced anapyrexia: tzenburg M, Albers KM, Koerber HR, Davis BM (2004)
implications and putative mediators. Annu Rev Physiol 64:263– Nociceptors lacking TRPV1 and TRPV2 have normal heat re-
288 sponses. J Neurosci 24:6410–6415
Tosini G, Menaker M (1996) The pineal complex and melatonin Woods HA, Harrison JF (2002) Interpreting rejections of the
affect the expression of the daily rhythm of behavioral thermo- beneficial acclimation hypothesis: when is physiological plas-
regulation in the green iguana. J Comp Physiol A 179:135–142 ticity adaptive? Evolution 56:1863–1866
Tosini G, Bertolucci C, Foà A (2001) The circadian system of Wright ML, Pikula A, Cykowski LJ, Kuliga K (1996) Effect of
reptiles: a multioscillatory and multiphotoreceptive system. melatonin on the anuran thyroid gland: follicle cell prolifera-
Physiol Behav 72:461–471 tion, morphometry, and subsequent thyroid hormone secretion
Turner N, Else PL, Hulbert AJ (2003) Docosahexaenoic acid in vivo after melatonin treatment in vivo. Gen Comp Endo-
(DHA) content of membranes determines molecular activity of crinol 103:182–191
the sodium pump: implications for disease and metabolism. Wu BJ, Hulbert AJ, Storlien LH, Else PL (2004) Membrane lipids
Naturwiss 90:521–523 and sodium pumps of cattle and crocodiles: an experimental
Viana F, de la Pena E, Belmonte C (2002) Specificity of cold test of the membrane pacemaker theory of metabolism. Am J
thermotransduction is determined by differential ionic channel Physiol 287:R633–R641
expression. Nat Neurosci 5:254–260 Zaar M, Larsen E, Wang T (2004) Hysteresis of heart rate and heat
Viswanath V, Story GM, Peier AM, Petrus MJ, Lee VM, Hwang exchange of fasting and postprandial savannah monitor lizards
SW, Patapoutian A, Jegla T (2003) Opposite thermosensor in (Varanus exanthematicus). Comp Biochem Physiol 137A:675–
fruitfly and mouse. Nature 423:822–823 682