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Respiratory Physiology & Neurobiology 154 (2006) 302–318

Respiratory cooling and thermoregulatory coupling in reptiles�

Glenn J. Tattersall ∗, Viviana Cadena, Matthew C. Skinner

Department of Biological Sciences, Brock University, St. Catharines, Ont., Canada L2S 3A1

Accepted 13 February 2006

bstract

Comparative physiological research on reptilies has focused primarily on the understanding of mechanisms of the control ofreathing as they relate to respiratory gases or temperature itself. Comparatively less research has been done on the possible linketween breathing and thermoregulation. Reptiles possess remarkable thermoregulatory capabilities, making use of behaviouralnd physiological mechanisms to regulate body temperature. The presence of thermal panting and gaping in numerous reptiles,oupled with the existence of head–body temperature differences, suggests that head temperature may be the primary regulatedariable rather than body temperature. This review examines the preponderance of head and body temperature differences ineptiles, the occurrence of breathing patterns that possess putative thermoregulatory roles, and the propensity for head andrain temperature to be controlled by reptiles, particularly at higher temperatures. The available evidence suggests that thesehermoregulatory breathing patterns are indeed present, though primarily in arid-dwelling reptiles. More importantly, however,t appears that the respiratory mechanisms that have the capacity to cool evolved initially in reptiles, perhaps as regulatory

echanisms for preventing overheating of the brain. Examining the control of these breathing patterns and their efficacy ategulating head or brain temperature may shed light on the evolution of thermoregulatory mechanisms in other vertebrates,amely the endothermic mammals and birds.

2006 Elsevier B.V. All rights reserved.

eywords: Respiratory cooling; Panting; Gaping; Thermoregulation; Countercurrent exchange; Evaporative water loss

� This paper is part of a special issue entitled “Frontiers in Compar-tive Physiology II: Respiratory Rhythm, Pattern and Responses tonvironmental Change”, guest edited by W.K. Milsom, F.L. Powellnd G.S. Mitchell.∗ Corresponding author. Tel.: +1 905 688 5550x4815;

ax: +1 905 688 1855.E-mail address: [email protected] (G.J. Tattersall).

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569-9048/$ – see front matter © 2006 Elsevier B.V. All rights reserved.doi:10.1016/j.resp.2006.02.011

. Introduction

The subject of reptilian thermoregulation has longeen of interest to comparative physiology. Rep-iles, in general, possess a wide array of behavioural

echanisms for modifying body temperature, includ-
ng basking, shuttling, postural changes, and eye-ulging (Bogert, 1959; Heath, 1970). They also pos-ess numerous physiological mechanisms that appearo serve as modulators rather than determinants of
mailto:[email protected]

dx.doi.org/10.1016/j.resp.2006.02.011

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G.J. Tattersall et al. / Respiratory Phy

ody temperature, including heart rate and thermal hys-eresis, peripheral circulatory adjustments, and even

odest thermogenesis (Seebacher and Franklin, 2005).ess extensively explored from a physiological per-pective is the issue of respiratory cooling in reptiles,lthough considerable research has been done on theotal rates of evaporative water loss in reptiles.

Respiratory cooling ultimately manifests from thevaporative water loss that occurs in the upper airwaysnd buccal cavity during breathing. This cooling canesult from: (1) a eupneic breathing pattern producingonstitutive cooling of nasal passages; (2) a shallow, butapid ventilatory pattern (e.g. panting) which shouldnduce more extensive cooling of the nasal passages;3) an open mouth gaping that increases the surfacerea for evaporation and presumably cools the buc-al cavity and/or entire upper airways. These latterreathing patterns are prevalent throughout the reptilesTable 1), unfortunately, the control of breathing pat-erns and neural regulation of ventilation in the contextf body temperature control are poorly understood. Aonsiderable amount of research into the potential ther-oregulatory function of panting and gaping occurred

n the 1970s, with little revisiting of these concepts,xcept for a few recent studies (DeNardo et al., 2004;orrell et al., 2005; Tattersall and Gerlach, 2005).

In this review, we will outline: (1) the occurrence ofegional temperature differences in reptiles and the cir-umstantial evidence suggesting that respiratory cool-ng helps to regulate brain temperature; (2) the types
nd prevalence of respiratory patterns that possessnown or probable thermoregulatory function in rep-iles; (3) review the known anatomical arrangementshat may help lead to the regulation of brain tempera-
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able 1resence and absence of gaping and panting in reptilian orders (and/or subo

eptilian order/suborder Prevalencea Thermoregulatory fun

estudines + −quamataSerpentes + −Lacertilia +++ +++

rocodilia ++ ++phenodonta ? ?

a Plus sign refers to relative prevalence or strength of response, question sikely thermoregulatory function.

& Neurobiology 154 (2006) 302–318 303

ure via respiratory mechanisms; (4) discuss the knownata on respiratory water loss in reptiles and how thisan translate into cooling of the airways and lead torain cooling. This review should shed light on whetherhe regulated thermoregulatory variable in reptiles israin temperature rather than body core or peripheralemperature. It would appear that in certain reptiles,anting and gaping are effective cooling mechanismshat help maintain non-lethal brain temperatures undereat stress. Furthermore, it is our hope that this reviewill stimulate research into the integration of reptilian

espiratory and thermoregulatory physiology.

. Head–body temperature gradients in reptiles

Reptiles are well known for their thermoregula-ory capabilities (Bogert, 1959; Heath, 1964b, 1970;empleton, 1971; Huey, 1974), exhibiting numerousehavioural and physiological mechanisms for regulat-ng relatively precise body temperature. The majorityf thermoregulatory studies, however, have measuredody or cloacal temperature, with less emphasis onhe regulation of head temperature. Measurements ofead or brain temperature have been made simulta-eously with body temperatures, although few studiesave manipulated brain temperature in order to exam-ne the role of central thermoreception in physiolog-cal or behavioural mechanisms of thermoregulationexcept for Cabanac et al., 1967; Hammel et al., 1967;
empleton, 1971; Crawford and Barber, 1974). To date,ost reptiles have been demonstrated a temperature
ifferential between the head and body, particularlyuring heating. Little emphasis, however, has been

rders)

ctiona References

Moll and Legler (1971)

Jacobson and Whitford (1971)Heatwole et al. (1973), Crawford and Kampe (1971),Firth and Heatwole (1976), Crawford et al. (1977)

Spotila et al. (1977)

ign refers to no known studies, minus sign means there is no known

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04 G.J. Tattersall et al. / Respiratory Phy

laced on examining and comparing head–body tem-erature differentials under altered thermal regimes,uch as radiant, convective or conductive heating, norave there been attempts to compare the nature of theseifferentials during heating and cooling. Alligators, forxample, exhibit different rates of head heating versusody heating, which is dependent on the degree of evap-rative cooling from the mouth (Spotila et al., 1977).umerous lizards have been shown to have a loweread temperature than core body temperature at highmbient temperatures (Webb et al., 1972), althoughead and brain temperatures are known to rise initiallyore rapidly than body temperature under a constant

eat source (Heath, 1964a, 1966). The tendency is forrain temperature to reach a critical value during heat-ng, and thereafter show similar or lower values thanody temperature. Webb et al. (1972) found that dur-ng artificial heating of three Australian lizards, heademperature was higher than or similar to body temper-ture; after panting was initiated, the head temperatureell below that of the body.

A large literature on internal temperature gradientsomes from snakes (Johnson, 1973, 1975; Hammerson,977; Gregory, 1990). For example, in field caughtoas, the slope of the relationship between oral (esti-ate of head) and cloacal temperature was usually less

han one, indicating regional temperature differencesith cooler head temperatures (Dorcas and Peterson,997). At ambient temperatures below preferred bodyemperatures, snakes had higher oral temperatures thanody temperatures; however, they possessed lowerral temperatures when ambient temperatures climbed.his suggests a combination of behavioural thermoreg-lation and physiological regulation to achieve regula-ion of head temperature (Dorcas and Peterson, 1997).ield and laboratory work on the taipan has shown

hat the maximum preferred head temperature was9 ◦C, whereas body temperature could reach as highs 40.5 ◦C under voluntary conditions (Johnson, 1975).imilar results have been observed in some Australianythons, where intense heating led to faster warmingf the head temperature, after which internal respira-ory cooling appeared to lead to a constant esophagealemperature, in spite of a continually climbing body
emperature (Webb and Heatwole, 1971).
Certain turtles have shown similar capacities foregional differences in body temperature. Under someonditions, box turtles have the capacity to keep core

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& Neurobiology 154 (2006) 302–318

ody temperature 10.5 ◦C below ambient temperature,hrough extensive evaporative water loss (Sturbaumnd Riedesel, 1974). In another study, in box turtlesoused at 40 ◦C, preoptic (i.e. hypothalamic) tem-erature stabilised at 1–2 ◦C below ambient temper-ture, even though cloacal temperature was less than◦C different from ambient temperature (Morgareidgend Hammel, 1975). Spontaneous rises in evapora-ive water loss (non-respiratory) at constant body tem-erature, were associated with decreases in preopticemperature (Morgareidge and Hammel, 1975), sug-esting that in turtles, brain temperature is the primaryegulated variable linked to evaporative cooling. Inwo Australian turtles, head temperature was observedo increase more rapidly than cloacal temperature.pon tear formation at higher ambient temperatures,owever, head temperature would fall below that ofloacal, sometimes by as much as 7 ◦C (Webb andohnson, 1972), suggesting that evaporative water lossas linked to head temperature regulation. Although

he mode of evaporation might differ among reptiles,he effect appears to be the same: head and brain tem-erature can be kept from reaching high and lethalevels.

The overall significance of respiratory evaporativeooling and its potential for the regulation of head tem-erature can be easily observed by a comparison ofhe external nasal surface temperature with the exter-al temperature of the head. From our own observationsnd from published observations (Tattersall et al., 2004;attersall and Gerlach, 2005), we have observed thatxternal surface temperature of the nasal region is typ-cally cooler than the head temperature, and more so atigher temperatures. This simple pattern was observedn a population of semi-wild tortoises (Geochelonearbonaria; Fig. 1A; Tattersall and Abe unpublishedbservations). In lizards, such as the bearded dragonsPogona vitticeps), we observed a slight external res-iratory cooling in normoxia (Fig. 1B), with a muchore profound external cooling in hypoxia as lizards

ngaged in more pronounced and longer bouts of ther-al gaping behaviour, suggestive of a regulated decline

n the so-called body temperature set-point (Tattersallnd Gerlach, 2005). Finally, in rattlesnakes, the exter-
al cooling effect is most pronounced, with surfaceasal temperatures in resting animals up to 2 ◦C lowerhan head or body temperature (Fig. 1C). This responses further accentuated under conditions of high activity

G.J. Tattersall et al. / Respiratory Physiology & Neurobiology 154 (2006) 302–318 305

Fig. 1. External nose temperatures (obtained using infrared thermal imaging) are linearly correlated with head temperature, though at highertemperatures, there is usually significant respiratory cooling. (A) Semi-wild tortoises (Geochelone carbonaria) exhibit cooler nose temperaturesat high head temperatures (closed circles, slope = 0.82, intercept = 2.94; personal observations, N = 16). (B) Bearded dragons (Pogona vitticeps)exhibit a similar cooler nose at higher head temperatures. Hypoxia (7% O2; open circles, slope = 0.83, intercept = 2.79) leads to an increase ingaping, leading to colder nose than observed in normoxia (filled circles, slope = 0.74, intercept = 7.48) (N = 14; data from Tattersall and Gerlach,2 spiratora t obser( n all thr

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005). (C) Rattlesnakes (Crotalus durrisius) exhibit a constitutive remeal (open circles, slope = 0.80, intercept = 2.73), compared to tha

N = 12; data from Tattersall et al., 2004). The dotted diagonal line i

Fig. 2D) or during the post-prandial period whenetabolic rate, heat production and ventilation are all

ighly elevated (Figs. 1C and 2C; Tattersall et al.,004). Interestingly, in all three species the slope ofhe relationship between external nasal temperature andead temperature was approximately 0.8, meaning thathe nose is typically cooler than the head, and to aimilar extent in the turtles, lizards and rattlesnakes.ombined with an elevated intercept in all cases, this

uggests that respiratory cooling under normal breath-ng conditions (i.e. not panting or gaping) is prevalent atll temperatures, but possibly only significant at highermbient temperatures where it would be expected thatespiratory cooing could exert its most physiologicallymportant role in cooling the brain. At these highermbient temperatures, it is still unclear whether respi-atory cooling (without the aid of panting or gaping)s a regulated mechanism or a mere consequence oflevated ventilation due to a high metabolism. Never-heless, the presence of a simple but effective coun-ercurrent mechanism for heat exchange in the headf reptiles (see section below on respiratory counter-urrent mechanisms) seems to indicate that respiratory
ooling is, at least partially, a regulated process.
In general, there appears to be a capacity for sepa-ate or partially separate regulation of head temperaturerom body temperature. The general consensus is that

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y cooling that is augmented when metabolic rate is raised followingved with fasted snakes (filled circles, slope = 0.83, intercept = 2.77)ee plots is the isothermal line.

rain temperature is more precisely regulated than bodyemperature, through a combination of behaviouralnd physiological processes (Heath, 1964a; Webb etl., 1972; Johnson, 1973; Gregory, 1990; Dorcas andeterson, 1997). At low ambient temperatures, due toehavioural thermoregulation and a lower thermal iner-ia of the head, brain temperature can often be seen toe higher than body temperature, whereas at highermbient temperatures, respiratory cooling via pantingr higher total ventilation, may lead to a cooler brainemperature than body temperature.

. Thermoregulatory functions of respiratoryatterns

Reptiles, as all ectotherms, exhibit a positive cor-elation between body temperature and metabolism.n general, the concomitant higher oxygen demandsmposed by this rise in metabolism are met through anncrease in overall ventilation (Crawford and Kampe,971; Frappell and Daniels, 1991). At temperaturesbove the preferred range, many lizards (Table 1)xhibit a drastic increase in breathing frequency in
ddition to a decrease in tidal volume, in a pattern thatas been described as panting (Dawson and Templeton,966; Frappell and Daniels, 1991). This is accompa-ied by an open mouth and protruding tongue, which

306 G.J. Tattersall et al. / Respiratory Physiology & Neurobiology 154 (2006) 302–318

Fig. 2. Thermal images (upper 4 panels) of snakes under different conditions (Tattersall and Abe, unpublished observations). The lower 4panels are outlines of the upper thermal images to provide reference images. (A) Front view of a rattlesnake (Crotalus durrisius) at the end ofa prolonged apnea showing barely perceptible head cooling; (B) front view of the same rattlesnake in (A) 4 s later, at the end of inspiration,demonstrating the rapid respiratory cooing reaching the external surfaces (temperature scale is similar in A and B); (C) a different rattlesnakeexhibiting significant respiratory cooling under high level of activity (active tail rattling); (D) a python that had previously exhibiting gapingbehaviour, demonstrating whole head cooling from rapid respiratory rates leading to high rates of evaporative water loss (temperature scale isthe same in C and D). The diagonal lines in the outline represent corrugated cardboard paper.

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nhances evaporative cooling through the respiratoryract and the oral surfaces (Dawson and Bartholomew,958; Crawford, 1972; Heatwole et al., 1973). Thisreathing pattern is comparable to that observed inany panting birds and mammals and is of clear ther-oregulatory value. The temperature at which the pant-

ng response is initiated has been denoted as the pantinghreshold (Table 2).

In some other species of lizards, skinks for exam-le, mouth gaping occurs at nearly lethal temperaturesnd is directly preceded or accompanied by uncoor-inated body movements and breathing spasms, andoncludes with the cessation of respiration (Veron andeatwole, 1970; Webb et al., 1972). In these species,aping takes place when death is already imminent andeems to present no thermoregulatory relevance. Pant-ng and gaping have also been observed in some snakesJacobson and Whitford, 1971), and turtles (Moll andegler, 1971), though no role in thermoregulation hasver been shown in these groups (Table 1).

Gaping can play an important thermoregulatory rolen some reptiles; open mouth breathing has been doc-mented in crocodilians and has been demonstrated toffectively reduce head temperature as well as heat gainy the head (Spotila et al., 1977). This strategy allowsor longer basking periods, permitting the body tem-erature to climb to preferred levels while preventinghe head from overheating. It has also been demon-trated in several lizards that panting has a greaterooling effect on the head than on the rest of the bodyCrawford et al., 1977). During heating, the chuckwallaSauromalus obesus) was capable of maintaining body
emperatures 1 ◦C and brain temperatures about 3 ◦Celow ambient (45 ◦C) for up to 8 h when allowed toant; this gradient was eliminated when the mouth of
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able 2ituations that alter or change panting/gaping thresholds in reptiles

ituation Response Species

ehydration Higher in dehydration Pogona barbypoxia Lower in hypoxia Basiliscus vi

Pogona sp.ircadian Higher during the day than at night Amphibolurueasonal Higher during the summer than during

the rest of the yearAmphiboluru

ex Lower in females than in males Amphiboluru

hreshold is defined as the lowest temperature at which panting or gaping o

& Neurobiology 154 (2006) 302–318 307

he panting lizard was taped shut (Crawford, 1972).n addition, head and body temperatures of the desertguana (Dipsosaurus dorsalis) were maintained 6 and◦C lower than an ambient temperature of 50 ◦C fort least 25 min via evaporative water loss from pant-ng (Dewitt, 1967). Nevertheless, the occurrence of

head–body temperature differential may not neces-arily demonstrate a tighter physiological control overrain temperature. Instead, it has been argued that thisay reflect differences in the physical thermal charac-

eristics of the head and the body, since the head warmsore quickly than the body (Pough and McFarland,

976), due to size differences and thermal inertia. How-ver, numerous studies have demonstrated rapid andubstantial changes in brain temperature with littlehange in body temperature immediately after the com-encement of panting and increased evaporative water

oss (Templeton, 1971; Crawford, 1972; Morgareidgend Hammel, 1975; Crawford et al., 1977). This wouldeem to cast doubt on circumstantial reasons being therimary explanation for the production of brain tem-eratures lower than body temperatures.

Gaping and panting are sometimes accompaniedy gular movements. Gular pumping (high amplitudeovements) and gular fluttering (high frequency move-ents) have been described for varanids and geckos,

espectively and are thought to aid in evaporative cool-ng by increasing convective heat loss (Webb et al.,972; Heatwole et al., 1973). Owerkowicz et al. (1999)emonstrated that savannah monitors (Varanus exan-hematicus) employ gular pumping during locomo-ion to assist in ventilation. Similar results have been
btained in varanid lizards where lung inflation can beargely assisted by buccal pumping (Al-Ghamdi et al.,001).
References

ata Parmenter and Heatwole (1975)ttatus, Iguana iguana, Dupre et al. (1986), Tattersall and

Gerlach (2005)s muricatus Chong et al. (1973)s muricatus Heatwole et al. (1975)

s muricatus, Pogona sp. Heatwole et al. (1973), Tattersall andGerlach (2005)

ccurs

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The panting response is controlled by both periph-ral and central nervous mechanisms but the relativemportance of each of these mechanisms is still a matterf debate. Although both play an important role in thenset and inhibition of panting there seems to be con-iderable variation between reptile species. In the desertguana, D. dorsalis, the panting response is primarily

odulated by head temperature. It is necessary for theranial fluids and head skin to reach very high temper-tures in order for panting to take place. Even at lethalnternal body and skin temperatures (with the exceptionf cranial skin) panting will not occur unless the tem-erature of the head is also relatively high (Templeton,971). In S. obesus the panting response is controlledy a very complex relationship between peripheralnd central nervous thermoreceptors; panting is notctivated unless the appropriate combination of skin,ody and brain temperatures takes place (Crawford andarber, 1974). They demonstrated that warming of therain, body or skin will all evoke panting, with con-inuous panting being exhibited under high heat loads.

ore significantly, the threshold for inducing pantingn S. obesus was lowest in the brain, followed by theody, and finally by the skin. This suggests that the mostensitive thermoreceptors are located centrally, and theeast sensitive are located peripherally. This arrange-

ent is similar to that observed in mammals (Simont al., 1986). These thermoreceptors act in a coordi-ated fashion, since a high brain temperature alone isot enough to induce panting; body temperature alsoas to be above 38 ◦C before panting can be inducedy brain heating, suggestive of a central integration ofhese thermal signals, most likely within the preopticegion of the hypothalamus.

The role of the pineal complex (consisting ofhe parietal and pineal organs) in lizard thermoreg-lation and in panting in particular has been wellstablished (Firth and Heatwole, 1976; Firth, 1979).emoval of the parietal organ (a photoreceptor located

n the dorsal midline of the brain) from Amphibolorusuricatus significantly reduced the panting thresh-ld during spring and summer, whereas shielding ofhe lateral eyes also lowered the panting threshold,ut to a lesser extent (Firth and Heatwole, 1976).
ye shielded-parietalectomised lizards had even loweranting thresholds than lizards that had undergone pari-talectomy or eye shielding alone (Firth and Heatwole,976), suggesting an additive effect on the influence
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& Neurobiology 154 (2006) 302–318

f the parietal organ and the lateral eyes in the con-rol of panting. In species that do not possess a parietalrgan, such as geckos, the influence of the lateral eyesn the control of panting is enhanced. It is plausible thathotic information from the environment is transmittedrom these photosensitive organs to the thermoregula-ory centers in the hypothalamus (Firth, 1979).

There is also evidence of diel and seasonal variationn the panting threshold of lizards. The circadian fluctu-tions follow the environmental temperatures encoun-ered throughout the day, the night values being signif-cantly lower than diurnal ones and noon values beinglightly higher than those of the rest of the day (Chongt al., 1973). The thermal preferences of lizards are alsof a circadian nature and follow a pattern similar tohat of the panting thresholds. This is evident in ther-

al gradient experiments where even under constantight conditions the diurnal selected temperatures sig-ificantly exceed night selected temperatures (Cowgellnd Underwood, 1979; Firth et al., 1989). There is alsoonsiderable seasonal variation in the panting thresh-lds of lizards; higher thresholds being exhibited in theummer than in the rest of the year (Table 2). Heatwolet al. (1975) showed that this circannual variation is pri-arily influenced by photoperiod and thermal acclima-

ion. Animals acclimated to constant light will exhibitrogressively higher panting thresholds with increas-ng temperature of acclimation. In addition, lizardscclimated to a 16-h light/8-h dark photoperiod displayignificantly higher panting thresholds than those accli-ated to 8-h light/16-h dark (Heatwole et al., 1975). Asresult, longer days and higher temperatures like thoseresent in the summer months lead to higher pantinghresholds, presumably as a result of a seasonal changen preferred body temperature set-point or its equiva-ent.

The degree to which certain factors will affect dif-erent aspects of the behavioural thermoregulation of aizard depends on the environment in which the animalives and the adaptations with which it is equipped. Theevel of dehydration experienced by a lizard, for exam-le, can be an important source for panting thresholdariation in species from xeric environments but not son species living in habitats where water is an abundant
esource. The panting threshold of the desert dwellingizard (Pogona barbata), is progressively elevated withncreasing levels of dehydration, with a higher increasen the panting threshold during the earlier stages of

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ehydration than during the later ones (Parmenter andeatwole, 1975). This adaptation to hot, dry habitats

llows these lizards to conserve water when it is mosteeded at the expense of thermoregulatory accuracy,s well as to sacrifice water balance in a situationhere temperature regulation is imperative. In species

dapted to habitats where water is readily available,uch as A. muricatus, dehydration does not have a sig-ificant effect on the panting threshold (Parmenter andeatwole, 1975).Environmental factors such as hypoxia can also alter

ifferent aspects of behavioural thermoregulation. Itas been well established that animals reduce their pre-erred body temperature under low oxygen conditionsWood and Gonzales, 1996). This hypoxic thermoreg-latory response serves as a protective mechanism forital organs by reducing oxygen requirements duringow availability and thus prolonging the survival ofhe animal. Hicks and Wood (1985) tested the pre-erred temperatures of seven species of lizard in a ther-al gradient under different levels of oxygen concen-

ration. Lizards subjected to hypoxic conditions (7%2) exhibited significantly lower selected temperatures

ompared to those tested under normoxic conditions.ot surprisingly, the thermal threshold for evaporative

ooling through gaping or panting is also lowered withecreasing concentrations of oxygen. When exposedo 7% oxygen, basilisks and green iguanas signifi-antly lower the body and skin temperature at whichanting is initiated (Dupre et al., 1986). Tattersall anderlach (2005) tested the effect of hypoxia on the over-

ll gaping time and the magnitude of the gape of theearded dragon, P. vitticeps and demonstrated that theagnitude of the opening of this lizard’s mouth dur-

ng gaping as well as the overall time employed inuch activity are also significantly affected by inspiredxygen levels. Progressively heating the animals whileimultaneously exposing them to different oxygen con-entrations causes the lizards to spend more time gap-ng during hypoxia than in normoxia. Tattersall anderlach (2005) also described three types of gape for

he bearded dragon according to the extent of the open-ng of the lizard’s mouth: Type I, a very small gape;ype II, a typical gape; Type III corresponded to a wide
pen mouth with protruding tongue. When beardedragons were exposed to low oxygen concentrations10 and 6%) progressively lower temperatures elicitedypes II and III gaping responses when compared to
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& Neurobiology 154 (2006) 302–318 309

ormoxic conditions. All of these respiratory responsesoint to a graded and regulated decline in the so-calledody temperature set-point.

Sex is also an important factor when considering theegulation of panting or gaping thresholds. Tattersallnd Gerlach (2005) showed that female bearded drag-ns consistently exhibited lower gaping thresholds thanales. This is consistent with the findings of Heatwole

t al. (1973) who found slightly higher, although notignificant, panting thresholds in male Jacky dragonsA. muricatus) than in females and also consistentith findings that sex can have subtle, albeit signifi-

ant effects on behavioural thermoregulation in reptilesLailvaux et al., 2003).

Apparent from the wide array of responses listedbove is that changes in the panting and gaping thresh-lds, although respiratory in nature, occur for a ther-oregulatory purpose (see also Tables 1 and 2). Fur-

hermore, although only briefly outlined here, the pant-ng and gaping responses in reptiles appear to have bothroportional and threshold properties, suggestive of aentral neural integrator and regulator (Simon et al.,986; Bligh, 1998). For example, the amount of time aizard spends engaged in thermoregulatory panting asell as the magnitude of the mouth gape increase with

ncreasing temperature (Tattersall and Gerlach, 2005).rawford and Barber (1974) also demonstrated that

he pattern of panting (intermittent versus continuous)perated in a graded fashion, becoming continuoushenever the thermal drive was high. Interestingly,

hat thermal drive could be derived from brain, body,r skin thermoreceptors. Combined, these two studiesoth suggest the existence of a proportional control inhe nature of the panting and gaping responses. In otherords, the degree to which these respiratory responsesanifest is proportional to the magnitude of the devi-

tion from the preferred or set-point temperature. Thiss a hallmark feature of a thermoregulatory effectoresponse.

. Cephalic blood flow and cardiovascularontrol of head temperature

As discussed earlier, it has been repeatedly observedhat when reptiles are basking or exposed to a high heattress environment, a head–body temperature gradientevelops (Dorcas and Peterson, 1997). This head–body

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emperature gradient can be attributed to a combinationf physical differences, behavioural thermoregulation,r physiological control (Dorcas and Peterson, 1997),s outlined above. This section will focus on the cardio-ascular mechanisms found within the cephalic regionhat may aid in the regulation of brain temperature. Ithould be pointed out, however, that it is currently notlear how cephalic blood flow regulation is linked toespiratory cooling.

Early work suggested that the reptilian brain exhibitsentrally thermosensitive neurons with a putative car-iovascular role (Rodbard et al., 1950), suggesting, athe time, that ectotherms possess similar central regula-ory mechanisms to endotherms. Subsequently, Heath1964a) observed that during basking in the hornedizard (Phrynosoma coronalum), the head warmed
p faster than the body, resulting in a head–bodyemperature gradient of approximately 2–4 ◦C. Thisas thought to be largely due to the larger surface
rea to volume ratio (Heath, 1964a, 1966; Pough and

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ig. 3. Cephalic blood supply in lizards that are involved in thermoregulan the left, in (A) (from Bruner, 1907), with small black arrows indicatingonstrictor muscle contracts, increasing venous pressure and causing a buiorcing blood to drain the head through the lateral commisure (L.C.), the exteountercurrent exchange between the internal jugular (I.J.) vein and the intermall arrows indicate direction of heat exchange.

& Neurobiology 154 (2006) 302–318

cFarland, 1976). Differential head and body heat-ng rates and at least transiently, head–body tempera-ure gradients, can be developed and maintained by aountercurrent heat exchanger. Similar to countercur-ent heat exchangers found in the extremities of manyarine animals, there is a cranial countercurrent heat

xchanger located in the head of reptiles (Heath, 1966).n this unique reptilian exchange system, there is heatxchange between the internal jugular vein and thenternal carotid artery controlled by the internal jugularonstrictor muscle (Fig. 3). During basking, the inter-al jugular carries warm blood away from the head, andue to its close proximity to the internal carotid artery,eat is transferred to the cooler carotid artery blood,hus retaining heat in the head (Oelrich, 1956; Heath,964a, 1966). Interestingly, when the body tempera-

◦
ure was increased to 30 C in P. coronalum, an eye-ulging phenomenon repeatedly occurred, resulting inhe diminishing of the head–body temperature gradient.his was followed by an increase in the heating rate of
tion. Cranial venous supply in the lizard (Lacerta agilis) is shownheat flow. Heath (1966) proposed (B, on right) that the jugularis

ld-up of blood in the cephalic venous sinuses (C.V.S.), eventuallyrnal jugular (E.J.) vein and the vertebral vein (V.V.). As a result, the

nal carotid artery is by-passed, and brain heating can be diminished.

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he body and a concurrent decrease in the rate of heat-ng in the head (Heath, 1964a). Eye-bulging indicateshat there has been an alteration in circulatory bloodow within the cephalic region (Fig. 3; Bruner, 1907;eath, 1964a; Crawford, 1972), and Heath (1964a)

uggested that the internal jugular constrictor mus-le transiently flexes at higher head temperatures. Theesult of this contraction is that blood now fills theephalic venous sinuses increasing the cephalic venousressure, manifesting externally as eye-bulging. Thencrease in pressure initiates the opening of cephalichunts, where blood flows through the external jugularein and vertebral veins, by-passing the normal flowhrough the internal jugular vein. Consequently, theres no heat exchange between the internal jugular veinnd the internal carotid artery. The elimination of theountercurrent heat exchange system allows for heatransfer from the head to the body, causing an increasen the body heating rate and a decrease in the heatingate within the head; this diminishes the head–bodyemperature gradient during the later phase of a baskingout (Heath, 1964a, 1966). Dewitt (1967) also noticedimilar eye protrusion behaviour in D. dorsalis, andhen eye-bulging occurred there was also a decline in

he head–body temperature gradient (i.e. a trend towardhe head temperature becoming equal to or less thanody temperature), suggesting a similar cardiovascu-ar mechanism to control the head–body temperatureradient.

A physiological countercurrent heat exchanger sys-em is advantageous in the cranium of reptiles in thatt allows for the brain to be quickly warmed up aftercool period; when the optimal temperature has been

urpassed, however, the temperature sensitive brain cane cooled or its heating rate slowed, by disabling theountercurrent heat exchanger and dumping its heat tohe body (Heath, 1966). The topic of thermoregulatory-elated countercurrent exchange mechanisms will beddressed in the following section.

. Respiratory countercurrent mechanisms

Many vertebrates have evolved physiological mech-
nisms to dissipate heat and cool the temperature sen-itive brain during high heat stress. One mechanismhat tends to be consistent across mammalian, aviannd possibly reptilian species is the countercurrent
ewro

& Neurobiology 154 (2006) 302–318 311

eat exchange system found within the respiratoryassages. Within the nasal passages of mammals andirds there are complex structures called turbinates.hese turbinates can be described as one or moreairs of coiled cartilage, covered with moist mucocil-ated epithelium (Hillenius, 1992, 1994; Geist, 2000;illenius and Ruben, 2004). Unlike mammals and birds

hat have relatively more complex turbinate structures,ost reptile species have relatively simple formations.he formations are termed conchae consisting of onlyfew coiled cartilaginous processes (Hillenius, 1992,994; Hillenius and Ruben, 2004). In D. dorsalis andther species, the conchae contain a salt gland (Murrishnd Schmidt-Nielsen, 1970; Schmidt-Nielsen et al.,970; Schmidt-Nielsen, 1972). Crocodilians have aore complex nasal passage than the rest of the rep-

ilian orders, having three conchae in succession downhe nasal passages (Hillenius, 1992, 1994).

To understand how respiratory nasal passages coulde utilised to cool the brain it is first useful to graspow the nasal passages and turbinates function inndotherms. The countercurrent heat exchangers foundn the nasal passages are analogous in function butot in flow to vascular heat exchangers. In vasculareat exchangers, blood flows in opposite directions andeat transfer occurs between the parallel arteries andeins. This process is referred to as spatial separationue to the close proximity of the two vessels (Jacksonnd Schmidt-Nielsen, 1964; Schmidt-Nielsen, 1972).owever, in the nasal passages there is only temporal

eparation that can be simply described as air flow thatoves in and out within one functional tube (Jackson

nd Schmidt-Nielsen, 1964; Schmidt-Nielsen, 1972).uring inspiration, the dry, cooler ambient air comes in

ontact with the coiled nasal turbinates which heat andaturate the incoming air. As the incoming air passesver the mucosal surfaces heat is lost from the moisturface and is gained by the air. This creates a coolerucosal surface which often falls below body tem-

erature (Jackson and Schmidt-Nielsen, 1964). Con-equently, due to evaporation, there is also water lossrom the nasal surface humidifying the passing air. Fol-owing inspiration, the incoming air is now at bodyemperature and fully saturated within the lungs. Upon
xpiration, the now warmed and humidified air in turnarms the cool mucosal surface created during inspi-
ation. As a result the warm air from the lung passesver the cool mucosal surfaces which regain the heat

3 siology

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rom the exhaled air that was lost during prior inspi-ation. Given that the air leaving the nasal passage iselow body temperature, water is conserved throughondensation on the mucosal surface, and thus the aireaving the nasal passage is no longer fully saturatedHillenius, 1992).

Although the preceding described how the nasal pas-ages and turbinates function in endotherms, it alsoemonstrated how heat and water can be conserved.hen mammals, birds, and reptiles are exposed to high

emperatures that may result in the overheating of therain, however, respiratory mechanisms may insteade utilised to dissipate heat rather than conserve it,hrough the stimulation of panting, gaping, and/or alter-ng cranial shunts, and thus by-passing respiratory andardiovascular countercurrent mechanisms.

Mammals, such as artiodactyls, utilise respiratoryooling along with vascular heat exchange systemso cool the brain. Taylor and Lyman (1972) demon-trated that gazelles were able to keep the brain 2.7 ◦Cooler than that of the body after body temperatureas raised by exercise. This was achieved by bloodessels in the mucosa being cooled by evaporation inhe nasal passageways. The cooled venous blood thenasses through the carotid rete which consists of a seriesf arterioles located inside the cranial cavity. This ishere the heat exchange occurs cooling the warm arte-

ial blood that is being directed to the brain (Baker,979, 1982; Jessen, 1998, 2001; Mitchell et al., 2002).arotid retes are most prominent in artiodactyls and

elids and their cooling capacity on the brain is some-hat limited. Generally in artiodactyls, the degree tohich the brain can be cooled by this means is less than◦C (Mitchell et al., 2002). Analogous to mammals,irds also use a combination of vascular countercur-ent heat exchange system. Similar to the mammalianarotid rete, birds utilise an opthalmic rete to aid inrain cooling (Baker, 1982; Mitchell et al., 2002). Likehe carotid rete, the opthalmic rete is a collection ofmall arteries developed from the carotid artery ands interwoven with the veins that drain the cool bloodorm buccopharyngeal surfaces and the beak (Baker,982; Fuller et al., 2003). Blood from the buccopha-yngeal mucosa and turbinates in the beak would be
ooled by evaporation during panting or gular flutter-ng (Zurovsky and Laburn, 1987).
Comparable to mammals and birds, but not as com-lex, reptiles also use a vascular countercurrent heat

trCg

& Neurobiology 154 (2006) 302–318

xchange system in combination with respiratory pas-ageways. Crawford (1972) recorded that when pantings initiated in S. obesus, a brain temperature 2.7 ◦Celow that of the body can be sustained during higheat stress (discussed in Sections 2 and 3). In S. obe-us, the carotid arteries are in close proximity to theurface of the pharynx and are exposed to air move-ent when panting. During panting the carotid artery is

ooled, thus simultaneously cooling the blood directedor the head. Webb et al. (1972) also noted that duringpen mouth gaping and gular fluttering (300 min−1)n geckos, the orbital sinuses were clearly engorgedith blood, suggesting that heat can be removed from

he vascular system directly through evaporation fromhe inner surfaces of the mouth near the blood sinuses.lthough there are no reports of reptiles with retia

ound near the carotid artery, there is a shunt systemhat occurs in the cranium (previously discussed). Withoth the vascular countercurrent heat exchange sys-em and respiratory mechanism working together, therain of some reptiles can be efficiently cooled duringigh environmental temperatures. Through the com-ined efforts of the constriction of the internal jugularonstrictor muscle and panting, the brain may not onlyower its rate of heating when reptiles are basking, butctually begin to cool at extreme temperatures. Due tohe fact that the head warms faster than the body (Poughnd McFarland, 1976), it is entirely plausible that aountercurrent heat exchange mechanism has evolvedo regulate the temperature sensitive brain in reptilesHeath, 1964a), particularly in those that are exposedo warm ambient temperatures and intense solar radia-ion that leads to high or lethal body temperatures.

. Respiratory evaporative water loss

The literature comparing standardised respiratoryater losses in reptiles is not very extensive, with most

vaporative water loss estimates being based primar-ly on whole body assessments. In a few instances, itas been possible to dissociate respiratory water lossrom total cutaneous water loss (see Table 3). To facil-tate comparisons of water loss from the respiratory
racts, the ratio of respiratory evaporative water lossate to metabolic rate (Respiratory Water Extractionoefficient = RWEC; mg H2O/mL O2) can be used. Itives an indication of the ability of the respiratory

G.J. Tattersall et al. / Respiratory Physiology & Neurobiology 154 (2006) 302–318 313

Table 3Respiratory water extraction coefficient (mg H2O/mL O2) in two different species of mammals and 4 different species of lizards

Species Tb (◦C) RWEC (mg H2O/mL O2) References

Kangaroo rat (Diplodomys spectabilis) 38a 0.57 Schmidt-Nielsen and Schmidt-Nielsen (1950)Albino rat (Rattus norvegicus) 38a 0.94 Schmidt-Nielsen and Schmidt-Nielsen (1950)

Pristidactylus torquatus 25 8.66b Labra and Rosenmann (1994)30 9.43b

Pristidactylus volcanensis 25 6.93b Labra and Rosenmann (1994)30 7.56b

Varanus sp. 25 0.26 Thompson and Withers (1997)38 0.93c

Chuckwalla (Sauromalus obesus) 26 0.61 Crawford and Kampe (1971)35 0.7040 1.24

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Estimated values based on approximate mammalian body tempeb Values calculated from data reported in the study of Labra and Rc 38 ◦C value extrapolated from 25 ◦C based on a Q10 of 2.6 obser

ystem to recover moisture derived from lung ventila-ion, while standardizing for the influence of metabolicate (Schmidt-Nielsen and Schmidt-Nielsen, 1950).he value has been extensively measured in mammals,ith values ranging from 0.4 in desert mammals to 1.0

n other mammals, including humans. The RWEC cane as low as 0.7–0.93 (Table 2) in some lizards, a valuehat is higher than the values of 0.4 observed by kanga-oo rats (Schmidt-Nielsen and Schmidt-Nielsen, 1950),esert mammals that possess countercurrent exchangeechanisms and elaborate respiratory turbinates. TheWEC of 0.7–0.93, however, is not dissimilar fromon-desert mammals with turbinates. Other reptilianalues range from 0.8 up to 10 (Table 3), suggestingwide range of values in the few reptiles where this

as been measured. It is apparent from the few stud-es that exist, that although the RWEC varies greatlyn reptiles, some values are at par with the standard

ammalian values, particularly in desert dwelling rep-iles. The reasons for the similar values between someeptiles and some endotherms is unclear at present, par-icularly because the absence of respiratory turbinatesn reptiles is thought to result in relatively high rates ofespiratory evaporative water loss (Hillenius, 1992). Its clear, however, from studies on mammals that pos-
ess respiratory turbinates, that cooling of respiratoryassages occurs, primarily for the purposes of recov-ring heat and moisture. Nevertheless, it is plausiblehat a cool respiratory passage would also serve to cool
cBio

nn (1994).ween 20 and 25 ◦C.

he brain if the appropriate circulatory arrangementsxist.

Except for Murrish and Schmidt-Nielsen (1970), itas been tacitly assumed that since most ectothermsave body temperatures close to ambient, they wouldave little need for recovering heat or moisture inhe respiratory passages. However, it would be pru-ent to consider the role of respiratory cooling aspossible moisture recovery mechanism, in addition

o any thermoregulatory role. Preliminary data (Tat-ersall and Andrade, unpublished observations) fromhe South American rattlesnake, Crotalus durissus,how that nasal air temperatures and head temperaturehange dramatically during inspiration and expirationn animals equilibrated under different thermal regimesFig. 4). At lower temperatures of 26 ◦C, head tem-erature is nearly identical to ambient temperature. Atigher ambient temperatures, the deviation betweenead and ambient grows larger, being approximately.2–0.4 ◦C lower at 30 ◦C and over 1.5 ◦C lower at anmbient temperature of 34 ◦C. These modest changesccurred at relative humidities between 40 and 70%. At0% relative humidity, the deviation between head andmbient temperature can be as large as 2 ◦C at a mod-rate ambient temperature of 30 ◦C due to the greater
apacity for evaporation, similar to that observed byorrell et al. (2005). The dynamic response result-
ng in this deviation in head temperature is the actf breathing. During inspiration, the nasal passage

3 siology

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ools to a value that can be up to 6 ◦C lower thanmbient temperature, indicating significant evapora-ion within the airways and cooling of the respiratoryalls. The shallower, more distal temperatures also

all, though only to a fraction of that of the deeper
irways. During non-ventilatory periods, the deep air-ays slowly and passively warm up toward ambient
emperature, whereas the shallow airways remain fairlyonstant. The entire airway, however, tends to remain

rbht

ig. 4. Deep (solid black line) and shallow (dark grey line) nasal temperaturemperatures (dotted line) (Tattersall and Andrade, unpublished observation

a is approximately 30 ◦C and relative humidity of 50%; (C) Ta is approxim0 ◦C with a low relative humidity of <10%. In (A–C) the breathing tracxpiration downwards. Dotted vertical lines indicate the onset of inspiration.nd Ta at higher breathing frequencies (which occur at higher Ta) and at low

& Neurobiology 154 (2006) 302–318

ooler than ambient or head temperature through-ut the non-ventilatory period. Continuous evapora-ion inside the airways is reduced once airflow hastopped, particularly as the airway humidity would belevated due to evaporation that occurred during inspi-
ation. Upon initiation of expiration in the subsequentreath, both deep and shallow airways warm up towardead temperature, which is slightly below ambientemperature.
es recorded in a rattlesnake (Crotalus durissius) at different ambients). (A) Ta is approximately 26 ◦C and relative humidity of 50%; (B)ately 34 ◦C and relative humidity of 50%; (D) Ta is approximately

e recorded by impedance is shown, with inspiration upwards andNote the larger gradient between head temperature (light grey line)relative humidity.

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During the entire breathing period, airway tempera-ure is always lower than head or ambient temperature,uggesting either continual evaporation during periodsf respiratory silence, or thermal inertia and sustainedooler temperatures due to the lack of air flow. The lat-er seems more likely, particularly given the subsequentapid increase in airway temperature during expiration.urthermore, there is a strong influence of depth in theares on ambient temperature changes, suggesting apatial thermal gradient as well as the temporal gradi-nt. This gradient may be crucial to the conservation ofater in many reptiles. This methodological approacharrants a more systematic approach in the future when

xamining the water conservation strategies of rep-iles, particularly given the preliminary nature of theseata. Although respiratory turbinates are absent in mosteptiles, it is possible that a slow and deep breathingattern can lead to the conditions necessary for signif-cant water recovery during normal breathing, as wells leading to some degree of brain temperature regu-ation coupled to respiratory cooling. Experiments thatimultaneously manipulate relative humidity and ambi-nt temperature, as in Borrell et al. (2005) might be ableo discern whether changes in breathing patterns playspecific role in thermoregulatory control of head or

ody temperature.On an evolutionary timescale, we would predict that

he greatest propensity for respiratory-induced cool-ng should occur in desert dwelling or xeric adaptedeptiles, particularly lizards, as seen from the fact thatanting and gaping appear to be most common in theseeptiles (Table 1) and are effective at regulating headr body temperature (Templeton, 1971; Crawford andarber, 1974). Murrish and Schmidt-Nielsen (1970)stimated that the desert iguana (Iguana iguana) recov-rs 31% of the respiratory water that would have beenost if no respiratory cooling existed. It is obvioushat although evaporation occurs in the respiratory pas-ages, not all moisture is lost to the atmosphere. Evapo-ation occurs primarily during inspiration and providesor additional cooling of the airways, and can serve theurpose of allowing for respiratory water to condenseuring expiration, as it does in mammalian turbinates.his is somewhat speculative, and thus the critical point

or future research would be to firmly establish theink between respiratory cooling, respiratory patternhanges, and the potential for regulation of brain tem-erature.

leto

& Neurobiology 154 (2006) 302–318 315

. Concluding remarks

Many reptiles appear to possess rather exquisite reg-lation of brain temperature, particularly in the facef high ambient temperatures. Although the best pre-ision seems to be restricted to certain lizards, ineneral, reptiles have acquired the necessary neuro-ogical pathways for sensing and regulating tempera-ure in the body (Bogert, 1959; Crawford and Barber,974; Morgareidge and Hammel, 1975; Grigg et al.,004). Indeed, it may even be the case that behaviouralnd physiological thermoregulation are aimed primar-ly at the maintenance or regulation of brain tem-erature rather than body temperature, as has beenidely assumed (Webb et al., 1972; Webb and Johnson,972; Hammerson, 1977; Gregory, 1990; Dorcas andeterson, 1997). From a sensory perspective, brain,ody and skin thermoreceptors can all activate pantingn certain reptiles, although brain temperature is the

ost sensitive regulator, evoking panting at lower tem-eratures than body or skin thermoreceptors (Crawfordnd Barber, 1974). This pattern of activation is quiteimilar to how mammalian thermoreceptors respond tohanging temperature and effect heat loss mechanismsRichards, 1970). As Crawford and Barber (1974)ointed out, it appears that reptiles possess the nec-ssary regulatory mechanisms, but not necessarily theapacity for robust regulation of core body temperature,s seen in the endothermic vertebrates. Continuouslyaintaining large temperature gradients between them-

elves and their environment is prohibitively expensiverom an osmoregulatory perspective, and thus respira-ory cooling may only reasonably be expected to coolhe brain.

We speculate, therefore, that respiratory cooling cane imparted to the brain through vascular mechanismsr simply via conductive heat transfer. In some reptiles,anting and gaping operates as an ambient temperature-ependent switch that is induced prior to high, lethalemperature exposure, often in a graded and regulatedashion. It has not escaped our notice that a pro-ound respiratory cooling could be most pronouncedn slower breathing, larger tidal volume reptiles, likenakes (Stinner, 1982; Andrade et al., 2004), since the
ow air velocity will ensure adequate time for heatxchange and phase changes of water to occur betweenissue and air. In addition, the long non-ventilatory peri-ds will further support the capacity for cool airways

ology

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Cowgell, J., Underwood, H., 1979. Behavioral thermoregulation inlizards: a circadian rhythm. J. Exp. Zool. 210, 189–194.

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D

D

D

D

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rawford, E.C., 1972. Brain and body temperatures in a pantinglizard. Science 177, 431–433.

rawford, E.C., Barber, B.J., 1974. Effects of core, skin, and braintemperature on panting in lizard Sauromalus obesus. Am. J. Phys-iol. 226, 569–573.

rawford Jr., E.C., Kampe, G., 1971. Physiological responses of thelizard Sauromalus obesus to changes in ambient temperature.Am. J. Physiol. 220, 1256–1260.

rawford, E.C., Palomeque, J., Barber, B.J., 1977. Physiologicalbasis for head–body temperature differences in a panting lizard.Comp. Biochem. Physiol. A 56, 161–163.

awson, W.R., Bartholomew, G.A., 1958. Metabolic and cardiacresponses to temperature in the lizard Dipsosaurus dorsalis.Physiol. Zool. 31, 100–111.

awson, W.R., Templeton, J.R., 1966. Physiological responses totemperature in the alligator lizard Gerrhonotus multicarinatus.Ecology 47, 759–765.

eNardo, D.F., Zubal, T.E., Hoffman, T.C.M., 2004. Cloacal evap-orative cooling: a previously undescribed means of increas-ing evaporative water loss at higher temperatures in a desertectotherm, the Gila monster Heloderma suspectum. J. Exp. Biol.207, 945–953.

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orcas, M.E., Peterson, C.R., 1997. Head–body temperature dif-ferences in free-ranging rubber boas. J. Herpetol. 31, 87–93.

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316 G.J. Tattersall et al. / Respiratory Physi

to play a role in cooling the brain. At present, the pos-sible role for changes in the eupneic breathing pattern(i.e. non-panting or gaping) that could produce greateror lesser respiratory cooling leading to the maintenanceof head temperature would be speculative, but certainlywarrants future investigation.

Acknowledgements

We would like to acknowledge Denis Andrade andAugust Abe for providing access to the rattlesnakesand tortoises. We would like to extend our gratitudeto Dimitri Skandalis for critically proofreading themanuscript, and significantly improving the final ver-sion. The authors’ research was funded by the NaturalSciences and Engineering Research Council of Canada,the Canadian Foundation for Innovation, and by a Pre-mier’s Research Excellence Award to G.J.T.

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respiratory cooling and thermoregulatory coupling in reptiles

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