REVIEW

Frank Seebacher Æ Craig E. Franklin

Physiological mechanisms of thermoregulation in reptiles: a review

Received: 15 February 2005 / Revised: 29 April 2005 / Accepted: 20 May 2005 / Published online: 27 July 2005� Springer-Verlag 2005

Abstract The thermal dependence of biochemical reac-tion rates means that many animals regulate their bodytemperature so that fluctuations in body temperature aresmall compared to environmental temperature fluctua-tions. Thermoregulation is a complex process that in-volves sensing of the environment, and subsequentprocessing of the environmental information. We sug-gest that the physiological mechanisms that facilitatethermoregulation transcend phylogenetic boundaries.Reptiles are primarily used as model organisms forecological and evolutionary research and, unlike inmammals, the physiological basis of many aspects inthermoregulation remains obscure. Here, we review re-cent research on regulation of body temperature, ther-moreception, body temperature set-points, andcardiovascular control of heating and cooling in reptiles.The aim of this review is to place physiological ther-moregulation of reptiles in a wider phylogenetic context.Future research on reptilian thermoregulation shouldfocus on the pathways that connect peripheral sensing tocentral processing which will ultimately lead to thethermoregulatory response.

Keywords Body temperature Æ Evolution ÆThermoreception Æ Endothermy Æ Ectothermy ÆMetabolism Æ Control Æ Heat Æ Cardiovascular

Abbreviations TRP: Transient receptor potential Æ NO:Nitric oxide Æ NOS: Nitric oxide synthase Æ COX:

Cyclooxygenase enzyme Æ CPT:8-Cyclopentyltheophylline

Introduction

The thermodynamic dependence of biochemical reactionrates makes thermal physiology the most pervasivecomponent in the biology of animals. There are twoprinciple, but not mutually exclusive, trajectories alongwhich the thermal physiology of vertebrate animals hasevolved. On the one hand, there is a trend towardsregulating body temperature very precisely within nar-row bounds regardless of environmental conditions(DiBona 2003). On the other trajectory, physiological/biochemical reaction rates have evolved to be plasticwithin individuals and/or between populations andspecies with the result that functional rates are main-tained despite considerable variation in body tempera-ture (Guderley and St. Pierre 2002; Johnston andTemple 2002; Guderley 2004).

In this review, we focus on the regulation of bodytemperature and the physiological mechanisms thatfacilitate thermoregulation, rather than thermal plastic-ity and temperature compensation of reaction rates. Theopportunity for thermoregulation is limited in thermallyhomogenous environments, particularly in water wherethe large convection coefficients rapidly equalise thermaldifferentials between an animal and its environment.Except for those animals that are very large or extremelywell-insulated, body temperature of aquatic organismstends to equal that of the water, and aquatic animalscompensate biochemically and physiologically for tem-porally varying body temperatures and/or their distri-bution is restricted to favourable climatic regions. Onland, daily regulation of body temperature is facilitatedby the heterogeneity of the thermal environment, andrelatively low heat transfer rates in air. Thermoregula-tion is a complex process that must integrate sensing oftemporal and spatial variation in the thermal environ-ment with behavioural and physiological responses that

Communicated by I.D. Hume

F. Seebacher (&)Integrative Physiology, School of Biological Sciences A08,University of Sydney, Sydney, NSW 2006, AustraliaE-mail: fseebach@bio.usyd.edu.auTel.: +61-2-93512779Fax: +61-2-93514119

C. E. FranklinSchool of Integrative Biology, The University of Queensland,St. Lucia, QLD 4072, Australia

J Comp Physiol B (2005) 175: 533–541DOI 10.1007/s00360-005-0007-1

will result in a narrow range of body temperatures rel-ative to operative temperatures fluctuations (Seebacherand Shine 2004).

The aim of this review is to summarise recent researchon physiological mechanisms of body temperature con-trol, and to place reptiles within the broader frameworkof vertebrate thermoregulation. Many traits of verte-brates are evolutionarily conservative, and the futuredirection in the field of reptilian thermal physiology canbe informed by the more intensive research efforts andresultant detailed knowledge of mammalian thermo-regulatory mechanisms. In the past 10–15 years, thecharacterisation of molecular mechanisms involved inthermoregulation, such as thermally sensitive proteinsand the various roles of nitric oxide, have been partic-ularly significant. Hence, we will review some of themore medically orientated literature on mammals alongwith recent work on reptiles.

We will first provide a general summary of thermo-regulatory mechanisms. Regulation of body temperaturepresupposes that animals are capable of sensing theirenvironment, and of processing information. Hence, thesecond and third section will review thermoreceptionand set-points of body temperature regulation. In thefinal section we will discuss cardiovascular mechanismsof temperature control which are an essential compo-nent of thermoregulation in both endotherms and ec-totherms.

Regulation of body temperature

The principle physiological basis of body temperatureregulation in endotherms is the production of metabolicheat in combination with thermal insulation (Kauffmanet al. 2001; Kvadesheim and Aarseth 2002; Seebacher2003). Compared to ectotherms, increased metabolicheat production in endotherms is in part owing to arelative increase in metabolically active tissues—liver,heart, and gastrointestinal systems (Fig. 1), to an in-crease in cellular density of mitochondria, and to thedecoupling of metabolic pathways from ATP produc-tion (Else and Hulbert 1981; Else and Hulbert 1985;Brand et al. 1991). Specific decoupling mechanisms, suchas leaky membranes and uncoupling proteins (Brand etal. 2004), lead to the electrochemical free-energy gener-ated across the mitochondrial membrane to be dissi-pated as heat rather than converted into chemical energyby oxidative phosphorylation (Kadenbach 2003).Uncoupling proteins are well-known from mammalsand birds (Nedergaard et al. 2001; Raimbault et al. 2001;Brand et al. 2004; Kabat et al. 2004) but have as yet notbeen reported from ectothermic reptiles.

The proportion of polyunsaturated fatty acids in thecomposition of mitochondrial membranes is correlatedwith the activity of membrane bound proteins. Mem-brane composition may, therefore, be a principalmechanism that regulates dissipation of the protongradient, and it may act as a metabolic pacemaker

(Hulbert and Else 1999; Else and Hulbert 2003). Ofparticular interest is docosahexaenoic acid (DHA) whichis an important modulator of membrane bound sodiumpump activity (Turner et al. 2003). Na+–K+ ATPaseconcentrations are similar in microsomal membranes ofa crocodile and a cow, but enzyme activities were 4–5fold greater in the cow compared to the crocodile(Fig. 1). Delipidation of Na+–K+ ATPase and recon-stitution with membranes across species (e.g. cow pro-tein with crocodile membrane) provides direct evidencethat protein activity is determined by the membranes(Wu et al. 2004). Additionally, endotherms have signif-icantly greater concentrations of DHA and other poly-unsaturated fatty acids compared to ectotherms (Brandet al. 1994; Wu et al. 2004) so that there is a correlationbetween protein activity and membrane fatty acidcomposition.

Although internal heat production is negligible forthermoregulation in ectothermic reptiles, metabolic heatmay be important for nest temperature regulation.Developing alligator embryos may produce sufficientmetabolic heat to raise the temperature at the centre ofan egg cluster to 2–3�C above that of an open arrange-ment of eggs (Ewert and Nelson 2003). Typically, how-ever, reptiles thermoregulate behaviourally by exploitingtheir thermal environment resulting in body tempera-tures that fall within a narrow range for at least part ofthe day (Hertz 1992; Hertz et al. 1993; Seebacher et al.2003; Seebacher and Shine 2004). Basking in the sun isone of the most typical thermal behaviours in reptiles(Cowles and Bogert 1944; Seebacher 1999; Gvozdik2002), although exposure to sun may have functionsother than thermoregulation. For example, the pantherchameleon’s (Furcifer pardalis) exposure to UV radia-tion functions at least partly in regulating endogenous

Fig. 1 Comparisons between a mammal and a reptile. Sodiumpump concentrations (pmol mg protein�1) are not significantlydifferent between cows and crocodiles, but the molecular activities(ATP/min) of the pumps are significantly greater in the cow (maingraph; data from Wu et al. 2004). The mass of the major organs(ratio lizard:mouse shown) is significantly lower in reptiles than inmammals (inset; data from Else and Hulbert 1981)

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vitamin D3 production (Ferguson et al. 2003; Fergusonet al. 2005). Photolytically produced vitamin D performsa number of physiological functions, including regula-tion of Ca2+ metabolism and cell signalling (Boyen et al.2002).

Thermoreception

The efficacy of behavioural thermoregulation dependson the capacity of animals to sense their thermal envi-ronment. Sensing of environmental temperatures wouldseem particularly important for animals that thermo-regulate behaviourally because the targeted exploitationof different thermal microhabitats requires contrastingof environmental and internal temperatures (Cooper2002). Specialised peripheral nerve endings that can re-spond to both constant and variable temperatures areknown from several invertebrate and vertebrate taxa(Cesare and McNaughton 1996; Caterina et al. 1997;Viana et al. 2002; Brown 2003; Patapoutian et al. 2003;Viswanath et al. 2003). In mammals, temperature maybe sensed by a family of transient receptor potential ionchannels (TRP) that are gated by specific temperatures(Viswanath et al. 2003). These thermally activated TRPsare located within the free nerve endings in the skin, butare also found in the peripheral nervous system, brain,heart and liver (Patapoutian et al. 2003). Six thermallysensitive TRPs have been identified that each operateover distinct temperature ranges (Fig. 2). Other trans-ducers that have been implicated in thermosensing inmammals include the two-pore domain K+ channels(TREK-1; Caley et al. 2005).

A different sensing mechanism exists in sharks wherethe electrosensitive ampullae of Lorenzini are capable ofsensing changes in environmental temperature (Brown2003). Gel-filled canals connect pores at the surface ofsharks to the innervated ampullae situated subdermally.The gel has the thermoelectric properties of a semicon-ductor, thereby conveying thermal information from theskin pores to the nerve endings in the ampullae (Brown2003).

The pineal complex may act as a thermal sensor inreptiles (Lutterschmidt et al. 1997), but specific neuralsensors associated with ion channels are not known fromreptiles. A possible exception are boid and crotalinesnakes that possess specific heat sensing organs (pit or-gans; de Cock Buning 1983). Pit organs are innervatedby the trigeminal nerve in a sensory pathway that in-volves protein kinase C as the signal transducer (Moonet al. 2003), and are capable of detecting electromagneticradiation from near UV to infrared (Moiseenkova et al.2003). The function of pit organs is thought to lie pri-marily in prey detection and capture (de Cock Buning1983; Shine and Sun 2002). The infrared receptors in thepit organs of the snake Trimeresurus flavoviridis aresensitive to temperature (Moon 2004), but their detec-tion distance is very short (<0.005 m; Jones et al. 2001)which would make it quite ineffective for predation

(Jones et al. 2001). Short detection distance could beadvantageous for thermoreception associated withthermoregulation. Behavioural trials with the rattle-snake, Crotalus atrox, indicate that pit organs are usedby the animals to detect thermally favourable micro-habitats. When snakes in a maze were given the choiceof a thermally stressful (40�C) or a benign (30�C) envi-ronment after being exposed initially to the stressfulenvironment, snakes with pit organs that were experi-mentally blocked chose the benign refuge on signifi-cantly fewer occasions than snakes with intact pit organs(Krochmal and Bakken 2003; Fig. 2). This pattern ofpreferentially choosing thermal refugia persisted across12 pit viper species all of which possess facial pits, butnot in a true viper that lacks facial pits (Krochmal et al.2004). Behavioural data therefore indicate that pit or-gans are multifunctional, and that thermoregulation

Fig. 2 Environmental sensing in vertebrates. a Heat stressedrattlesnakes, Crotalus atrox, with intact pit organs (before) hadsignificantly greater success (proportion of all trials) in choosing athermally benign habitat than snakes with blocked pit organs(blocked); when pit organs were unblocked (after), snakes regainedthe ability to choose the benign habitat. A success rate of 0.5 wouldbe expected if choice was random. Data from Krochmal andBakken (2003). b Alligators and crocodiles possess dome pressuresensors (blue arrow) on their head that are innervated by thetrigeminal nerve (Soares 2002; photo of Crocodylus johnstoni byFS). cMammals possess a family of transient receptor potential ionchannels (TRPV1–4, TRPV8, ANKTM1) each of which has adifferent thermal sensitivity range. Data from Patapoutian et al.(2003)

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rather than prey detection may even have been theprinciple selection pressure leading to their evolution(Krochmal et al. 2004).

Pit organs are the only known thermal sensors amongnon-avian reptiles, although crocodilians possess exter-nal pressure sensors, or dome pressure receptors (Soares2002; Fig. 2). Dome pressure receptors are dome likestructures located on the head of crocodilians that arecovered externally by a considerably reduced keratinlayer, and which are innervated by the trigeminal nerve(Soares 2002). The mechanisms of transduction ofpressure stimuli within the receptors are unknown—is itpossible that dome receptors also sense heat maybe via asemiconductor mechanism?

Body temperature set-points

Body temperatures in thermoregulating reptiles mayvary temporally within individuals between day andnight and between seasons, and many species becomeinactive when ‘‘preferred’’ body temperatures are unat-tainable. Daily and seasonal fluctuations in behaviourand physiological functions of reptiles—as well as ofother vertebrates—are regulated by the circadian sys-tem. The circadian system acts as an endogenous oscil-lator by integrating the hypothalamus, lateral eyes, thepineal complex (Tosini et al. 2001), and, at least inmammals, the retina (Sakamoto et al. 2004). Thermallyinspired behaviour in reptiles may be hormonally di-rected, and melatonin in particular has been associatedwith thermoregulation. Melatonin is produced by thepineal gland and interacts with the thyroid gland, and itmay directly influence secretions of thyroid hormone(Krotewicz and Lewinski 1994; Wright et al. 1996).Melatonin may act as an intermediary between opticalsignals, and behavioural and physiological responses(Axelrod 1974). Levels of melatonin characteristic tothose produced in darkness have been observed to de-crease the body temperature selected by a snake (Pit-uophis melanoleucus; Lutterschmidt et al. 1997; Fig. 3).Similar responses whereby selected body temperaturesare influenced by concentration of melatonin occur inseveral species of reptile (e.g. Cothran and Hutchison1979; Erskine and Hutchison 1981). Additionally, mel-atonin levels also vary seasonally and may, therefore, actto co-ordinate activity and thermoregulation with cli-matic conditions on a daily and seasonal time scale(Mendoca et al. 1995; Tosini and Menaker 1996).Interestingly, however, intraperitoneal injections ofmelatonin did not affect body temperature selection of anocturnal snake (Lamprophis fuliginosus) in a linearthermal gradient compared to control treatments (Lut-terschmidt et al. 2002; Fig. 3). Thermoregulatorybehaviour in toads also does not depend on melatonin(Sievert and Poore 1995), and these findings may indi-cate that there are fundamental differences in thermalcontrol centers between diurnal and nocturnal ecto-therms.

Selected body temperatures may be influenced byenvironmentally induced changes in metabolic state. Inparticular, low blood oxygen concentrations, eitherbrought about by intensive exercise or a hypoxic envi-ronment can result in lower body temperatures (anapy-rexia) in ectotherms and endotherms (Wagner andGleeson 1997; Steiner and Branco 2002; Petersen et al.2003). Hypoxia increases adenosine release which mayinteract with receptors on the hypothalamus to effect adecrease in body temperature (Barros and Branco 1999).For example, the selected body temperature of the lizardAnolis sagrei is 34.8�C under normoxic conditions, butexposure to hypoxic conditions in a thermal gradientresulted in a significant 5�C drop in selected body tem-peratures. Similarly, mean selected body temperaturesdecreased by 4�C following exhaustive exercise. Intra-peritoneal administration of the adenosine receptorantagonist 8-cyclopentyltheophylline prevented or sub-stantially reduced the hypoxia or exercise-induced dropin mean selected body temperature (Petersen et al. 2003;Fig. 4). However, administration of the adenosineantagonist did not reduce selected body temperatureduring normoxia (Petersen et al. 2003), and the reduc-tion in body temperature during hypoxia may be amechanism to reduce O2 consumption.

Nitric oxide (NO), and the activity of nitric oxidesynthase (NOS), is instrumental in the brain of mam-mals as a signalling molecule in the thermal response.Inhibition of NOS by injection of inhibitors directly intothe lateral cerebral ventricle of rats caused a significanthyperthermia that was sustained for several hours(Mathai et al. 2004). Intravenous injection of the NOSinhibitor L-NAME did not affect thermoregulation,however, demonstrating that NO acts specifically in thebrain (Mathai et al. 2004). Interestingly, inhibitingprostaglandin synthesis by administration of a non-ste-roidal anti-inflammatory drug (indomethacin) before theL-NAME treatment abolished the hyperthermic effect ofNOS inhibition (Mathai et al. 2004). The activity of

Fig. 3 After treatment with melatonin, the diurnal bullnakePituophis melanoleucus selected significantly lower body tempera-tures in a thermal gradient. In contrast, melatonin injection did notalter the body temperature selection of the nocturnal African housesnake Lamprophis fuliginosus (Data from Lutterschmidt et al. 2002)

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cyclooxygenase enzyme (COX), which is responsible forprostaglandin synthesis, may be controlled by NO(Salvemini 1997), and the interaction between theindomethacin and L-NAME treatments (Mathai et al.2004) show that the NOS–NO–COX control axis isimportant for thermoregulation in rats. The role ofprostaglandins in body temperature control and fever inmammals is well-established (Feldberg and Saxena1971), and direct injection of PGE2 into the hypotha-lamic region of the rat brain causes an increase in thethermogenic response (Madden and Morrison 2004).Nitric oxide synthase is present in the brains of a turtle(Bruning et al. 1994) and a lizard (Smeets et al. 1997),but whether it functions in thermoregulation remainsunknown. Prostaglandins, on the other hand, alter thethermoregulatory set-point in an amphibian (Bicego etal. 2002) and a reptile (Bernheim and Kluger 1976) bymediating a behavioural fever response following injec-tion of an exogenous pyrogen. In the toad, Bufo pa-racnemis, experimental lesions to the preoptic area of thebrain abolishes the characteristic pyrogen-induced feverresponse (Bicego and Branco 2002), and it seems likelythat the prostaglandin-mediated reaction is situated inthe preoptic area. Additionally, both prostaglandins andnitric oxide are important in cardiovascular responsesduring thermoregulation in reptiles (see below; Seeb-acher and Franklin 2003; Seebacher and Franklin2004a).

Cardiovascular control of heat transfer

The efficacy of behavioural thermoregulation is deter-mined to a large extent by cardiovascular changes(Bartholomew and Tucker 1963; Grigg et al. 1979; Griggand Seebacher 1999; Seebacher and Grigg 2001; Dzia-lowski and O’Connor 2001). It is advantageous forreptiles that regulate body temperatures within a narrow

range relative to environmental (operative) temperaturefluctuations to control rates of heating and cooling whilemoving in a thermally heterogeneous environment(Seebacher 2000). Such control may be achieved byaltering cardiac output and the distribution of bloodflow in the body. Elevated cardiac output, achievedprimarily by increase in heart rate in reptiles, andperipheral circulation will increase rates of transient heattransfer between animals and their environment(O’Connor 1999; Seebacher 2000; Seebacher andFranklin 2004b). Hence, by increasing heart rates duringheating and decreasing heart rates during cooling rep-tiles can exert control over heat exchange with theenvironment (Fig. 5). This pattern, known as heart ratehysteresis, has been described from all major lineages ofreptile (Bartholomew and Tucker 1963; Grigg et al.1979). Interestingly, in crocodiles (Crocodylus porosus)the magnitude of the hysteresis (i.e. difference in heartrate between heating and cooling) depends on the modeby which heat is transferred between the animal and itsenvironment. The heart rate differential between heatingand cooling is greatest during radiant heating, and heartrate changes in proportion to the heat load experiencedat the animal surface (Franklin and Seebacher 2003;Fig. 5). By analogy, similar cardiovascular changes arethe principle thermoregulatory mechanisms whenendothermic body temperatures are within the thermalneutral zone (Romanovsky et al. 2002).

Preferential blood flow to the limbs during heating,supported by increased cardiac output, may be one ofthe mechanisms by which differential rates of heatingand cooling are achieved. Placing thermal insulationaround the limbs of Iguana iguana during heating andcooling did not alter rates of heat exchange compared toa control group, but a significant interaction betweenheating/cooling and insulated/uninsulated limbs indi-cates that limbs may be important in determining ratesof heating (Dzialowski and O’Connor 2004). Feedingand digestion causes an increase in heart rate even be-yond that resulting from heat. The additional cardiacoutput in postprandial Varanus exanthematicus did not,however, increase rates of heating and increased bloodflow after a meal appeared to be directed to the gutwithout any thermoregulatory effect (Zaar et al. 2004).

Heart rate hysteresis consists of two phases, one avery rapid (seconds) increase or decrease in heart rate inresponse to application or removal of heat, respectively,that occurs while body temperature remains stable. Thisrapid response, which may represent a neural reflex arc,is followed by a more gradual change in heart rate that isproportional to changes in body temperature, and dur-ing which heart rates during heating exceeds heart rateduring cooling at any given body temperature (Franklinand Seebacher 2003). The rapid-response phase is atleast partly controlled by cholinergic and b-adrenergicreceptors, but autonomic blockade did not abolish thehysteresis pattern in a lizard (Pogona barbata, Seebacherand Franklin 2001). A second control system that mayact either alongside or instead of the autonomic nervous

Fig. 4 Oxygen limitation induces anapyrexia in the lizard Anolissagrei. Body temperature selected in a thermal gradient wassignificantly lower in hypoxic air (10% O2) compared to normoxia.Similarly, selected body temperatures were decreased followingexhaustive exercise. Blockade of adenosine receptors with 8-cyclopentyltheophylline (CPT), however, significantly reduced theanapyrexia following hypoxia and exercise. Data from Petersen etal. (2003)

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system are prostaglandins. Prostaglandin F2a and pros-tacyclin cause a significant response in heart rate, andinhibition of prostaglandins abolishes the characteristicheart rate hysteresis response in the lizard Pogona vitti-ceps (Seebacher and Franklin 2003). In contrast, inhi-bition of cyclooxygenase enzyme did not affect heart ratedifferential during heating and cooling in Crocodylus

porosus, and heart rate hysteresis persisted even withdouble inhibition of nitric oxide synthase and cycloox-ygenase enzyme (Seebacher and Franklin 2004a). Nitricoxide did play a role during heating and cooling in C.porosus, by buffering blood pressure against changes inheart rate during cooling (Seebacher and Franklin2004a).

The differences in the role of prostaglandins betweenlineages (Squamata [P. vitticeps] and Archosauria [C.porosus]) may indicate an evolutionary divergence ofcontrol systems. The existence of heart rate hysteresisduring heating and cooling in a crustacean (Goudkampet al. 2004) indicates that this phenomenon may haveevolved alongside arterialisation of the vascular systemin organisms with principle regulatory mechanisms inplace. In the subsequent evolution of heart rate hysteresisas a thermoregulatory trait different mechanisms thatcontrol the cardiovascular system during thermoregula-tion may have taken precedence in different lineages.

Conclusions and future directions

Thermoregulation is an integrated process involvingperipheral sensing, central processing, and co-ordinationof response functions that will affect body temperature.Recent advances in thermal reception and temperaturecontrol in non-reptilian vertebrates, particularly inmammals, could inform the field of reptilian thermo-regulation and guide future research efforts. The evolu-tionary conservatism of many traits among vertebratessuggests that there may exist a commonality of ther-moregulatory mechanisms as well. Ectothermy is anancestral trait and comparisons between modern taxasuggest that endotherms utilise many of the same prin-ciple mechanisms of thermoregulation as ectotherms(e.g. Else and Hulbert 1981).

Knowledge of thermoregulation in reptiles is con-centrated on behavioural and ecological aspects and,despite the recent advances reviewed here, some of theessential mechanisms that underlie the whole animalresponse remain poorly understood. There are severaltraits known to be important in thermoregulation ofendotherms but not of ectothermic reptiles, e.g. uncou-pling proteins, thermally sensitive proteins and neurons,and the central control function of NO and COX. Atpresent, these differences probably reflect the disparateresearch efforts on the respective groups rather thanevolutionary differences. Significant advances in under-standing the evolution of thermoregulation will be madewhen similarities and differences between differentgroups of animals (endotherms–ectotherms, avian–nonavian reptiles, vertebrates–invertebrates, etc.) have beenexperimentally established. Selection pressures act onindividual traits rather than on composite, whole animalresponses (Woods and Harrison 2002). To understandthe evolution of thermoregulation, it is essential tounderstand the mechanisms that underlie the thermalresponses that are characteristic for each group.

Fig. 5 Reptiles control rates of heating and cooling by changingheart rates (fH) and cardiac output. a fH is significantly higherduring heating compared to cooling (data from Seebacher andFranklin 2003). b Modelled body temperatures for different heartrates; increased heart rates lead to faster rates of heating anddecreased heart rates slow cooling. Body temperatures were modelaccording to methods in Seebacher (2000). c Changes in heart rate(D fH) during heating and cooling (excluding the ‘‘reflex’’ period)depend on the heat load received at the animal surface (curve:Y=6.41*1.06x ; R2=0.74). Data from Franklin and Seebacher(2003)

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Future research on reptilian thermoregulation shouldfocus on the pathways that connect peripheral sensing tocentral processing which will ultimately lead to the ther-moregulatory response. Sensing of the thermal environ-ment is particularly important for behaviouralthermoregulation, and although the pineal complex andmelatonin provide a mechanism to process environmen-tal conditions, it seems likely that there also exist other,peripheral sensors. For example, restricted local heatingof a dorsal section in a crocodile and a lizard elicited adistinct cardiovascular response (Morgareidge andWhite1972; Grigg and Alchin 1976) that must have been inde-pendent from direct stimulation of the pineal. Rather, wespeculate that peripheral thermal sensors are present inreptiles, and these sensors may be similar to the inner-vated thermal sensor proteins found in mammals andDrosophila (Patapoutian et al. 2003). Central processingof the peripheral thermal information may involve theNOS–NO–COX axis that could integrate set-points andcardiovascular control. It is of particular interest that thecardiovascular response to heating and cooling in reptilesis at least in part mediated by the integration between thebaroreflex and systemically acting NOS and COX en-zymes (Altimiras et al. 1998; Seebacher and Franklin2003; Seebacher and Franklin 2004a). A link between thelocal and central functions of COX and NOmay connectenvironmental stimuli to the heart rate hysteresis that istypical of reptilian thermoregulation.

Acknowledgments This work was supported by an Australian Re-search Council Discovery grant to F.S. and C.E.F.

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