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J Comp Physiol B (2005) 175: 533541

DOI 10.1007/s00360-005-0007-1

R EV IE W

Frank Seebacher 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 reaction rates means that many animals regulate their body
temperature so that uctuations in body temperature are
small compared to environmental temperature uctuations. 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:

Communicated by I.D. Hume


F. Seebacher (&)
Integrative Physiology, School of Biological Sciences A08,
University of Sydney, Sydney, NSW 2006, Australia
E-mail: fseebach@bio.usyd.edu.au
Tel.: +61-2-93512779
Fax: +61-2-93514119
C. E. Franklin
School of Integrative Biology, The University of Queensland,
St. Lucia, QLD 4072, Australia

Cyclooxygenase enzyme CPT:


8-Cyclopentyltheophylline

Introduction
The thermodynamic dependence of biochemical reaction
rates makes thermal physiology the most pervasive
component in the biology of animals. There are two
principle, but not mutually exclusive, trajectories along
which the thermal physiology of vertebrate animals has
evolved. On the one hand, there is a trend towards
regulating body temperature very precisely within narrow bounds regardless of environmental conditions
(DiBona 2003). On the other trajectory, physiological/
biochemical reaction rates have evolved to be plastic
within individuals and/or between populations and
species with the result that functional rates are maintained despite considerable variation in body temperature (Guderley and St. Pierre 2002; Johnston and
Temple 2002; Guderley 2004).
In this review, we focus on the regulation of body
temperature and the physiological mechanisms that
facilitate thermoregulation, rather than thermal plasticity and temperature compensation of reaction rates. The
opportunity for thermoregulation is limited in thermally
homogenous environments, particularly in water where
the large convection coecients rapidly equalise thermal
dierentials between an animal and its environment.
Except for those animals that are very large or extremely
well-insulated, body temperature of aquatic organisms
tends to equal that of the water, and aquatic animals
compensate biochemically and physiologically for temporally varying body temperatures and/or their distribution is restricted to favourable climatic regions. On
land, daily regulation of body temperature is facilitated
by the heterogeneity of the thermal environment, and
relatively low heat transfer rates in air. Thermoregulation is a complex process that must integrate sensing of
temporal and spatial variation in the thermal environment with behavioural and physiological responses that

534

will result in a narrow range of body temperatures relative to operative temperatures uctuations (Seebacher
and Shine 2004).
The aim of this review is to summarise recent research
on physiological mechanisms of body temperature control, and to place reptiles within the broader framework
of vertebrate thermoregulation. Many traits of vertebrates are evolutionarily conservative, and the future
direction in the eld of reptilian thermal physiology can
be informed by the more intensive research eorts and
resultant detailed knowledge of mammalian thermoregulatory mechanisms. In the past 1015 years, the
characterisation of molecular mechanisms involved in
thermoregulation, such as thermally sensitive proteins
and the various roles of nitric oxide, have been particularly signicant. Hence, we will review some of the
more medically orientated literature on mammals along
with recent work on reptiles.
We will rst provide a general summary of thermoregulatory mechanisms. Regulation of body temperature
presupposes that animals are capable of sensing their
environment, and of processing information. Hence, the
second and third section will review thermoreception
and set-points of body temperature regulation. In the
nal section we will discuss cardiovascular mechanisms
of temperature control which are an essential component of thermoregulation in both endotherms and ectotherms.

Regulation of body temperature


The principle physiological basis of body temperature
regulation in endotherms is the production of metabolic
heat in combination with thermal insulation (Kauman
et al. 2001; Kvadesheim and Aarseth 2002; Seebacher
2003). Compared to ectotherms, increased metabolic
heat production in endotherms is in part owing to a
relative increase in metabolically active tissuesliver,
heart, and gastrointestinal systems (Fig. 1), to an increase in cellular density of mitochondria, and to the
decoupling of metabolic pathways from ATP production (Else and Hulbert 1981; Else and Hulbert 1985;
Brand et al. 1991). Specic decoupling mechanisms, such
as leaky membranes and uncoupling proteins (Brand et
al. 2004), lead to the electrochemical free-energy generated across the mitochondrial membrane to be dissipated as heat rather than converted into chemical energy
by oxidative phosphorylation (Kadenbach 2003).
Uncoupling proteins are well-known from mammals
and birds (Nedergaard et al. 2001; Raimbault et al. 2001;
Brand et al. 2004; Kabat et al. 2004) but have as yet not
been reported from ectothermic reptiles.
The proportion of polyunsaturated fatty acids in the
composition of mitochondrial membranes is correlated
with the activity of membrane bound proteins. Membrane composition may, therefore, be a principal
mechanism that regulates dissipation of the proton
gradient, and it may act as a metabolic pacemaker

Fig. 1 Comparisons between a mammal and a reptile. Sodium


pump concentrations (pmol mg protein 1) are not signicantly
dierent between cows and crocodiles, but the molecular activities
(ATP/min) of the pumps are signicantly greater in the cow (main
graph; data from Wu et al. 2004). The mass of the major organs
(ratio lizard:mouse shown) is signicantly lower in reptiles than in
mammals (inset; data from Else and Hulbert 1981)

(Hulbert and Else 1999; Else and Hulbert 2003). Of


particular interest is docosahexaenoic acid (DHA) which
is an important modulator of membrane bound sodium
pump activity (Turner et al. 2003). Na+K+ ATPase
concentrations are similar in microsomal membranes of
a crocodile and a cow, but enzyme activities were 45
fold greater in the cow compared to the crocodile
(Fig. 1). Delipidation of Na+K+ ATPase and reconstitution with membranes across species (e.g. cow protein with crocodile membrane) provides direct evidence
that protein activity is determined by the membranes
(Wu et al. 2004). Additionally, endotherms have significantly greater concentrations of DHA and other polyunsaturated fatty acids compared to ectotherms (Brand
et al. 1994; Wu et al. 2004) so that there is a correlation
between protein activity and membrane fatty acid
composition.
Although internal heat production is negligible for
thermoregulation in ectothermic reptiles, metabolic heat
may be important for nest temperature regulation.
Developing alligator embryos may produce sucient
metabolic heat to raise the temperature at the centre of
an egg cluster to 23C above that of an open arrangement of eggs (Ewert and Nelson 2003). Typically, however, reptiles thermoregulate behaviourally by exploiting
their thermal environment resulting in body temperatures that fall within a narrow range for at least part of
the day (Hertz 1992; Hertz et al. 1993; Seebacher et al.
2003; Seebacher and Shine 2004). Basking in the sun is
one of the most typical thermal behaviours in reptiles
(Cowles and Bogert 1944; Seebacher 1999; Gvozdik
2002), although exposure to sun may have functions
other than thermoregulation. For example, the panther
chameleons (Furcifer pardalis) exposure to UV radiation functions at least partly in regulating endogenous

535

vitamin D3 production (Ferguson et al. 2003; Ferguson


et al. 2005). Photolytically produced vitamin D performs
a number of physiological functions, including regulation of Ca2+ metabolism and cell signalling (Boyen et al.
2002).

Thermoreception
The ecacy of behavioural thermoregulation depends
on the capacity of animals to sense their thermal environment. Sensing of environmental temperatures would
seem particularly important for animals that thermoregulate behaviourally because the targeted exploitation
of dierent thermal microhabitats requires contrasting
of environmental and internal temperatures (Cooper
2002). Specialised peripheral nerve endings that can respond to both constant and variable temperatures are
known 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 may
be sensed by a family of transient receptor potential ion
channels (TRP) that are gated by specic temperatures
(Viswanath et al. 2003). These thermally activated TRPs
are located within the free nerve endings in the skin, but
are also found in the peripheral nervous system, brain,
heart and liver (Patapoutian et al. 2003). Six thermally
sensitive TRPs have been identied that each operate
over distinct temperature ranges (Fig. 2). Other transducers that have been implicated in thermosensing in
mammals include the two-pore domain K+ channels
(TREK-1; Caley et al. 2005).
A dierent sensing mechanism exists in sharks where
the electrosensitive ampullae of Lorenzini are capable of
sensing changes in environmental temperature (Brown
2003). Gel-lled canals connect pores at the surface of
sharks to the innervated ampullae situated subdermally.
The gel has the thermoelectric properties of a semiconductor, thereby conveying thermal information from the
skin pores to the nerve endings in the ampullae (Brown
2003).
The pineal complex may act as a thermal sensor in
reptiles (Lutterschmidt et al. 1997), but specic neural
sensors associated with ion channels are not known from
reptiles. A possible exception are boid and crotaline
snakes that possess specic heat sensing organs (pit organs; de Cock Buning 1983). Pit organs are innervated
by the trigeminal nerve in a sensory pathway that involves protein kinase C as the signal transducer (Moon
et al. 2003), and are capable of detecting electromagnetic
radiation from near UV to infrared (Moiseenkova et al.
2003). The function of pit organs is thought to lie primarily in prey detection and capture (de Cock Buning
1983; Shine and Sun 2002). The infrared receptors in the
pit organs of the snake Trimeresurus avoviridis are
sensitive to temperature (Moon 2004), but their detection distance is very short (<0.005 m; Jones et al. 2001)
which would make it quite ineective for predation

Fig. 2 Environmental sensing in vertebrates. a Heat stressed


rattlesnakes, Crotalus atrox, with intact pit organs (before) had
signicantly greater success (proportion of all trials) in choosing a
thermally benign habitat than snakes with blocked pit organs
(blocked); when pit organs were unblocked (after), snakes regained
the ability to choose the benign habitat. A success rate of 0.5 would
be expected if choice was random. Data from Krochmal and
Bakken (2003). b Alligators and crocodiles possess dome pressure
sensors (blue arrow) on their head that are innervated by the
trigeminal nerve (Soares 2002; photo of Crocodylus johnstoni by
FS). c Mammals possess a family of transient receptor potential ion
channels (TRPV14, TRPV8, ANKTM1) each of which has a
dierent thermal sensitivity range. Data from Patapoutian et al.
(2003)

(Jones et al. 2001). Short detection distance could be


advantageous for thermoreception associated with
thermoregulation. Behavioural trials with the rattlesnake, Crotalus atrox, indicate that pit organs are used
by the animals to detect thermally favourable microhabitats. When snakes in a maze were given the choice
of a thermally stressful (40C) or a benign (30C) environment after being exposed initially to the stressful
environment, snakes with pit organs that were experimentally blocked chose the benign refuge on signicantly fewer occasions than snakes with intact pit organs
(Krochmal and Bakken 2003; Fig. 2). This pattern of
preferentially choosing thermal refugia persisted across
12 pit viper species all of which possess facial pits, but
not in a true viper that lacks facial pits (Krochmal et al.
2004). Behavioural data therefore indicate that pit organs are multifunctional, and that thermoregulation

536

rather than prey detection may even have been the


principle selection pressure leading to their evolution
(Krochmal et al. 2004).
Pit organs are the only known thermal sensors among
non-avian reptiles, although crocodilians possess external pressure sensors, or dome pressure receptors (Soares
2002; Fig. 2). Dome pressure receptors are dome like
structures located on the head of crocodilians that are
covered externally by a considerably reduced keratin
layer, and which are innervated by the trigeminal nerve
(Soares 2002). The mechanisms of transduction of
pressure stimuli within the receptors are unknownis it
possible that dome receptors also sense heat maybe via a
semiconductor mechanism?

Body temperature set-points


Body temperatures in thermoregulating reptiles may
vary temporally within individuals between day and
night and between seasons, and many species become
inactive when preferred body temperatures are unattainable. Daily and seasonal uctuations in behaviour
and physiological functions of reptilesas well as of
other vertebratesare regulated by the circadian system. The circadian system acts as an endogenous oscillator by integrating the hypothalamus, lateral eyes, the
pineal complex (Tosini et al. 2001), and, at least in
mammals, the retina (Sakamoto et al. 2004). Thermally
inspired behaviour in reptiles may be hormonally directed, and melatonin in particular has been associated
with thermoregulation. Melatonin is produced by the
pineal gland and interacts with the thyroid gland, and it
may directly inuence secretions of thyroid hormone
(Krotewicz and Lewinski 1994; Wright et al. 1996).
Melatonin may act as an intermediary between optical
signals, and behavioural and physiological responses
(Axelrod 1974). Levels of melatonin characteristic to
those produced in darkness have been observed to decrease the body temperature selected by a snake (Pituophis melanoleucus; Lutterschmidt et al. 1997; Fig. 3).
Similar responses whereby selected body temperatures
are inuenced by concentration of melatonin occur in
several species of reptile (e.g. Cothran and Hutchison
1979; Erskine and Hutchison 1981). Additionally, melatonin levels also vary seasonally and may, therefore, act
to co-ordinate activity and thermoregulation with climatic conditions on a daily and seasonal time scale
(Mendoca et al. 1995; Tosini and Menaker 1996).
Interestingly, however, intraperitoneal injections of
melatonin did not aect body temperature selection of a
nocturnal snake (Lamprophis fuliginosus) in a linear
thermal gradient compared to control treatments (Lutterschmidt et al. 2002; Fig. 3). Thermoregulatory
behaviour in toads also does not depend on melatonin
(Sievert and Poore 1995), and these ndings may indicate that there are fundamental dierences in thermal
control centers between diurnal and nocturnal ectotherms.

Fig. 3 After treatment with melatonin, the diurnal bullnake


Pituophis melanoleucus selected signicantly lower body temperatures in a thermal gradient. In contrast, melatonin injection did not
alter the body temperature selection of the nocturnal African house
snake Lamprophis fuliginosus (Data from Lutterschmidt et al. 2002)

Selected body temperatures may be inuenced by


environmentally induced changes in metabolic state. In
particular, low blood oxygen concentrations, either
brought about by intensive exercise or a hypoxic environment can result in lower body temperatures (anapyrexia) in ectotherms and endotherms (Wagner and
Gleeson 1997; Steiner and Branco 2002; Petersen et al.
2003). Hypoxia increases adenosine release which may
interact with receptors on the hypothalamus to eect a
decrease in body temperature (Barros and Branco 1999).
For example, the selected body temperature of the lizard
Anolis sagrei is 34.8C under normoxic conditions, but
exposure to hypoxic conditions in a thermal gradient
resulted in a signicant 5C drop in selected body temperatures. Similarly, mean selected body temperatures
decreased by 4C following exhaustive exercise. Intraperitoneal administration of the adenosine receptor
antagonist 8-cyclopentyltheophylline prevented or substantially reduced the hypoxia or exercise-induced drop
in mean selected body temperature (Petersen et al. 2003;
Fig. 4). However, administration of the adenosine
antagonist did not reduce selected body temperature
during normoxia (Petersen et al. 2003), and the reduction in body temperature during hypoxia may be a
mechanism to reduce O2 consumption.
Nitric oxide (NO), and the activity of nitric oxide
synthase (NOS), is instrumental in the brain of mammals as a signalling molecule in the thermal response.
Inhibition of NOS by injection of inhibitors directly into
the lateral cerebral ventricle of rats caused a signicant
hyperthermia that was sustained for several hours
(Mathai et al. 2004). Intravenous injection of the NOS
inhibitor L-NAME did not aect thermoregulation,
however, demonstrating that NO acts specically in the
brain (Mathai et al. 2004). Interestingly, inhibiting
prostaglandin synthesis by administration of a non-steroidal anti-inammatory drug (indomethacin) before the
L-NAME treatment abolished the hyperthermic eect of
NOS inhibition (Mathai et al. 2004). The activity of

537

Fig. 4 Oxygen limitation induces anapyrexia in the lizard Anolis


sagrei. Body temperature selected in a thermal gradient was
signicantly lower in hypoxic air (10% O2) compared to normoxia.
Similarly, selected body temperatures were decreased following
exhaustive exercise. Blockade of adenosine receptors with 8cyclopentyltheophylline (CPT), however, signicantly reduced the
anapyrexia following hypoxia and exercise. Data from Petersen et
al. (2003)

cyclooxygenase enzyme (COX), which is responsible for


prostaglandin synthesis, may be controlled by NO
(Salvemini 1997), and the interaction between the
indomethacin and L-NAME treatments (Mathai et al.
2004) show that the NOSNOCOX control axis is
important for thermoregulation in rats. The role of
prostaglandins in body temperature control and fever in
mammals is well-established (Feldberg and Saxena
1971), and direct injection of PGE2 into the hypothalamic region of the rat brain causes an increase in the
thermogenic 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 remains
unknown. Prostaglandins, on the other hand, alter the
thermoregulatory set-point in an amphibian (Bicego et
al. 2002) and a reptile (Bernheim and Kluger 1976) by
mediating a behavioural fever response following injection of an exogenous pyrogen. In the toad, Bufo paracnemis, experimental lesions to the preoptic area of the
brain abolishes the characteristic pyrogen-induced fever
response (Bicego and Branco 2002), and it seems likely
that the prostaglandin-mediated reaction is situated in
the preoptic area. Additionally, both prostaglandins and
nitric oxide are important in cardiovascular responses
during thermoregulation in reptiles (see below; Seebacher and Franklin 2003; Seebacher and Franklin
2004a).

Cardiovascular control of heat transfer


The ecacy of behavioural thermoregulation is determined to a large extent by cardiovascular changes
(Bartholomew and Tucker 1963; Grigg et al. 1979; Grigg
and Seebacher 1999; Seebacher and Grigg 2001; Dzialowski and OConnor 2001). It is advantageous for
reptiles that regulate body temperatures within a narrow

range relative to environmental (operative) temperature


uctuations to control rates of heating and cooling while
moving in a thermally heterogeneous environment
(Seebacher 2000). Such control may be achieved by
altering cardiac output and the distribution of blood
ow in the body. Elevated cardiac output, achieved
primarily by increase in heart rate in reptiles, and
peripheral circulation will increase rates of transient heat
transfer between animals and their environment
(OConnor 1999; Seebacher 2000; Seebacher and
Franklin 2004b). Hence, by increasing heart rates during
heating and decreasing heart rates during cooling reptiles can exert control over heat exchange with the
environment (Fig. 5). This pattern, known as heart rate
hysteresis, has been described from all major lineages of
reptile (Bartholomew and Tucker 1963; Grigg et al.
1979). Interestingly, in crocodiles (Crocodylus porosus)
the magnitude of the hysteresis (i.e. dierence in heart
rate between heating and cooling) depends on the mode
by which heat is transferred between the animal and its
environment. The heart rate dierential between heating
and cooling is greatest during radiant heating, and heart
rate changes in proportion to the heat load experienced
at the animal surface (Franklin and Seebacher 2003;
Fig. 5). By analogy, similar cardiovascular changes are
the principle thermoregulatory mechanisms when
endothermic body temperatures are within the thermal
neutral zone (Romanovsky et al. 2002).
Preferential blood ow to the limbs during heating,
supported by increased cardiac output, may be one of
the mechanisms by which dierential rates of heating
and cooling are achieved. Placing thermal insulation
around the limbs of Iguana iguana during heating and
cooling did not alter rates of heat exchange compared to
a control group, but a signicant interaction between
heating/cooling and insulated/uninsulated limbs indicates that limbs may be important in determining rates
of heating (Dzialowski and OConnor 2004). Feeding
and digestion causes an increase in heart rate even beyond that resulting from heat. The additional cardiac
output in postprandial Varanus exanthematicus did not,
however, increase rates of heating and increased blood
ow after a meal appeared to be directed to the gut
without any thermoregulatory eect (Zaar et al. 2004).
Heart rate hysteresis consists of two phases, one a
very rapid (seconds) increase or decrease in heart rate in
response to application or removal of heat, respectively,
that occurs while body temperature remains stable. This
rapid response, which may represent a neural reex arc,
is followed by a more gradual change in heart rate that is
proportional to changes in body temperature, and during which heart rates during heating exceeds heart rate
during cooling at any given body temperature (Franklin
and Seebacher 2003). The rapid-response phase is at
least partly controlled by cholinergic and b-adrenergic
receptors, but autonomic blockade did not abolish the
hysteresis pattern in a lizard (Pogona barbata, Seebacher
and Franklin 2001). A second control system that may
act either alongside or instead of the autonomic nervous

538

porosus, and heart rate hysteresis persisted even with


double inhibition of nitric oxide synthase and cyclooxygenase enzyme (Seebacher and Franklin 2004a). Nitric
oxide did play a role during heating and cooling in C.
porosus, by buering blood pressure against changes in
heart rate during cooling (Seebacher and Franklin
2004a).
The dierences in the role of prostaglandins between
lineages (Squamata [P. vitticeps] and Archosauria [C.
porosus]) may indicate an evolutionary divergence of
control systems. The existence of heart rate hysteresis
during heating and cooling in a crustacean (Goudkamp
et al. 2004) indicates that this phenomenon may have
evolved alongside arterialisation of the vascular system
in organisms with principle regulatory mechanisms in
place. In the subsequent evolution of heart rate hysteresis
as a thermoregulatory trait dierent mechanisms that
control the cardiovascular system during thermoregulation may have taken precedence in dierent lineages.

Conclusions and future directions

Fig. 5 Reptiles control rates of heating and cooling by changing


heart rates (fH) and cardiac output. a fH is signicantly higher
during heating compared to cooling (data from Seebacher and
Franklin 2003). b Modelled body temperatures for dierent heart
rates; increased heart rates lead to faster rates of heating and
decreased heart rates slow cooling. Body temperatures were model
according to methods in Seebacher (2000). c Changes in heart rate
(D fH) during heating and cooling (excluding the reex 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)

system are prostaglandins. Prostaglandin F2a and prostacyclin cause a signicant response in heart rate, and
inhibition of prostaglandins abolishes the characteristic
heart rate hysteresis response in the lizard Pogona vitticeps (Seebacher and Franklin 2003). In contrast, inhibition of cyclooxygenase enzyme did not aect heart rate
dierential during heating and cooling in Crocodylus

Thermoregulation is an integrated process involving


peripheral sensing, central processing, and co-ordination
of response functions that will aect body temperature.
Recent advances in thermal reception and temperature
control in non-reptilian vertebrates, particularly in
mammals, could inform the eld of reptilian thermoregulation and guide future research eorts. The evolutionary conservatism of many traits among vertebrates
suggests that there may exist a commonality of thermoregulatory mechanisms as well. Ectothermy is an
ancestral trait and comparisons between modern taxa
suggest that endotherms utilise many of the same principle mechanisms of thermoregulation as ectotherms
(e.g. Else and Hulbert 1981).
Knowledge of thermoregulation in reptiles is concentrated on behavioural and ecological aspects and,
despite the recent advances reviewed here, some of the
essential mechanisms that underlie the whole animal
response remain poorly understood. There are several
traits known to be important in thermoregulation of
endotherms but not of ectothermic reptiles, e.g. uncoupling proteins, thermally sensitive proteins and neurons,
and the central control function of NO and COX. At
present, these dierences probably reect the disparate
research eorts on the respective groups rather than
evolutionary dierences. Signicant advances in understanding the evolution of thermoregulation will be made
when similarities and dierences between dierent
groups of animals (endothermsectotherms, aviannon
avian reptiles, vertebratesinvertebrates, etc.) have been
experimentally established. Selection pressures act on
individual traits rather than on composite, whole animal
responses (Woods and Harrison 2002). To understand
the evolution of thermoregulation, it is essential to
understand the mechanisms that underlie the thermal
responses that are characteristic for each group.

539

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. Sensing of the thermal environment is particularly important for behavioural
thermoregulation, and although the pineal complex and
melatonin provide a mechanism to process environmental conditions, it seems likely that there also exist other,
peripheral sensors. For example, restricted local heating
of a dorsal section in a crocodile and a lizard elicited a
distinct cardiovascular response (Morgareidge and White
1972; Grigg and Alchin 1976) that must have been independent from direct stimulation of the pineal. Rather, we
speculate that peripheral thermal sensors are present in
reptiles, and these sensors may be similar to the innervated thermal sensor proteins found in mammals and
Drosophila (Patapoutian et al. 2003). Central processing
of the peripheral thermal information may involve the
NOSNOCOX axis that could integrate set-points and
cardiovascular control. It is of particular interest that the
cardiovascular response to heating and cooling in reptiles
is at least in part mediated by the integration between the
baroreex and systemically acting NOS and COX enzymes (Altimiras et al. 1998; Seebacher and Franklin
2003; Seebacher and Franklin 2004a). A link between the
local and central functions of COX and NO may connect
environmental stimuli to the heart rate hysteresis that is
typical of reptilian thermoregulation.
Acknowledgments This work was supported by an Australian Research Council Discovery grant to F.S. and C.E.F.

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