Professional Documents
Culture Documents
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
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:
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.
535
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
536
537
538
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
539
References
Altimiras J, Franklin CE, Axelsson M (1998) Relationship between
blood pressure and heart rate in the salt water crocodile Crocodylus porosus. J Exp Biol 201:22352242
Axelrod J (1974) The pineal gland: a neurochemical transducer.
Science 184:13411348
Barros RCH, Branco LGS (1999) Role of central adenosine in the
respiratory and thermoregulatory responses to hypoxia. Neuroreport 11:193197
Bartholomew GA, Tucker VA (1963) Control of changes in body
temperature, metabolism, and circulation by the agamid lizard,
Amphibolurus barbatus. Physiol Zool 36:199218
Bernheim HA, Kluger MJ (1976) Fever and antipyresis in the lizard
Dipsosaurus dorsalis. Am J Physiol 231:198203
Bicego KC, Branco LGS (2002) Discrete electrolytic lesion of the
preoptic area prevents LPS-induced behavioral fever in toads. J
Exp Biol 205:35133518
Bicego KC, Steiner AA, Antunes-Rodrigues J, Branco LGS (2002)
Indomethacin impairs LPS-induced behavioral fever in toads. J
Appl Physiol 93:512516
Boyen BD, Sylvia VL, Dean DD, Schwartz Z (2002) Membrane
mediated signalling mechanisms are used dierentially by
metabolites of vitamin D3 in musculoskeletal cells. Steroids
67:421427
Brand MD, Couture P, Else PL, Withers KW, Hulbert AJ (1991)
Evolution of energy metabolism. Biochem J 275:8186
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:181188
540
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 4:95103
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 266:12911297
Guderley H (2004) Metabolic responses to low temperature in sh
muscle. Biol Rev 79:409427
Guderley H, St. Pierre J (2002) Going with the ow or life in the
fast lane: contrasting mitochondrial responses to thermal
change. J Exp Biol 205:22372249
Gvozdik L (2002) To heat or to save time? Thermoregulation in the
lizard Zootoca vivipara (Squamata: lacertidae) in dierent
thermal environments along an altitudinal gradient. Can J Zool
80:479492
Hertz PE (1992) Temperature regulation in Puerto Rican
Anolis lizards: a eld test using null hypotheses. Ecology
73:14051417
Hertz PE, Huey RB, Stevenson RD (1993) Evaluating temperature
regulation by eld-active ectotherms: the fallacy of the inappropriate question. Am Nat 142:796818
Hulbert AJ, Else PL (1999) Membranes as possible pacemakers of
metabolism. J Theor Biol 199:257274
Johnston IA, Temple GK (2002) Thermal plasticity of skeletal
muscle phenotype in ectothermic vertebrates and its signicance
for locomotory behaviour. J Exp Biol 205:23052322
Jones BS, Lynn WF, Stone MO (2001) Thermal modeling of snake
infrared reception: evidence for limited detection range. J Theor
Biol 209:201211
Kabat AP, Rose RW, West AK (2004) Molecular identication of
uncoupling proteins 2 and 3 in a carnivorous marsupial, the
Tasmanian devil (Sarcophilus harrisii). Physiol Biochem Zool
77:109115
Kadenbach B (2003) Intrinsic and extrinsic uncoupling of oxidative
phosphorylation. Biochim Biophys Acta 1604:7794
Kauman A, Cabrera A, Zucker I (2001) Energy intake and fur in
summer- and winter-acclimated Siberian hamsters (Phodopus
sungorus). Am J Physiol 281:R519R527
Krochmal AR, Bakken GS (2003) Thermoregulation is the pits: use
of thermal radiation for retreat site selection by rattlesnakes. J
Exp Biol 206:25392545
Krochmal AR, Bakken GS, LaDuc TJ (2004) Heat in evolutions
kitchen: evolutionary perspectives on the functions and origin
of the facial pit of pitvipers (Viperidae: Crotalinae). J Exp Biol
207:42314238
Krotewicz M, Lewinski A (1994) Thyroid hormone secretion in
male Wistar rats treated with melatonin and/or thyrotropin;
dependence of eects on the used doses. Neuroendocrin Lett
16:263268
Kvadsheim PH, Aarseth JJ (2002) Thermal function of phocid seal
fur. Mar Mamm Sci 18:952962
Lutterschmidt DI, Lutterschmidt WI, Hutchison VH (1997) Melatonin and chlorpromazine: thermal selection and metabolic
rate in the bullsnake, Pituophis melanoleucus. Comp Biochem
Physiol C 118:271277
Lutterschmidt DI, Lutterschmidt WI, Ford NB, Hutchison VH
(2002) Behavioral thermoregulation and the role of melatonin
in a nocturnal snake. Horm Behav 41:4150
Madden CJ, Morrison SF (2004) Excitatory amino acid receptors
in the dorsomedial hypothalamus mediate prostaglandinevoked thermogenesis in brown adipose tissue. Am J Physiol
286:R320R325
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 29:401405
Mendoca MT, Tousignant AJ, Crews D (1995) Seasonal changes
and annual variability in daily plasma melatonin in the redsided garter snake (Thamnophis sirtalis parietalis). Gen Comp
Endocrinol 100:226237
Moiseenkova V, Bell B, Motamedi M, Wozniak E, Christensen B
(2003) Am J Physiol 284:R598R606
541
catecholaminergic neuronal structures in the brain of the lizard
Gekko gecko. J Comp Neurol 377:121141
Soares D (2002) An ancient sensory organ in crocodilians. Nature
417:241242
Steiner AA, Branco LSG (2002) Hypoxia-induced anapyrexia:
implications and putative mediators. Annu Rev Physiol 64:263
288
Tosini G, Menaker M (1996) The pineal complex and melatonin
aect the expression of the daily rhythm of behavioral thermoregulation in the green iguana. J Comp Physiol A 179:135142
Tosini G, Bertolucci C, Foa` A (2001) The circadian system of
reptiles: a multioscillatory and multiphotoreceptive system.
Physiol Behav 72:461471
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 90:521523
Viana F, de la Pena E, Belmonte C (2002) Specicity of cold
thermotransduction is determined by dierential ionic channel
expression. Nat Neurosci 5:254260
Viswanath V, Story GM, Peier AM, Petrus MJ, Lee VM, Hwang
SW, Patapoutian A, Jegla T (2003) Opposite thermosensor in
fruity and mouse. Nature 423:822823