Panting thresholds of lizards—I. Some methodological and internal influences on the panting threshold of an agamid, Amphibolurus muricatus

Camp. Biochem. Physic& 1973, VoI. 46A, pp. 799 to 826. Pergmwn Press. Printed in

Gmzt

Britain

PANTING THRESHOLDS OF LIZARDS-I. SOME METHODOLOGICAL AND INTERNAL INFLUENCES ON THE PANTING THRESHOLD OF AN AGAMID, AMPHIBOLURUS MURICATUS HAROLD

HEATWOLE,

BRUCE

T. FIRTH

and GRAHAME

J. W. WEBB

Department of Zoology, University of New England, Armidale, N.S.W. Australia

2351,

(Received 20 November, 1972)

Abstract-l. Amphibolurus muricatus undergoes thermal panting at body temperatures of approximately 40°C. 2. Body size, site of temperature measurement, sex, moulting and rate and method of heating did not significantly influence the panting threshold. 3. Rapid heating resulted in greater variability of panting threshold. 4. Non-radiant heat caused greater variation in panting threshold than radiant heat. 5. Repeated testing with short intervals between tests decreased panting threshold, whereas long intervals had no effect. 6. Panting was weakly developed in &inks and snakes tested. 7. The major source of variation in panting threshold is a day-to-day shift within individuals.

INTRODUCTION

exceptions are known, many species of lizards open the mouth widely when subjected to heat stress (see Table 1). In some, this response occurs only at the point that breathing nearly or completely ceases, heart beat precipitously drops and the animal approaches heat-induced spasms (Veron & Heatwole, 1970; Webb et al., 1972); such gaping can scarcely be of thermoregulatory significance. However, in other species the mouth is open during periods of high ventilation and would seem to be of use in enhancing evaporative cooling (Langlois, 1902; Cole, 1943 ; Dawson & Templeton, 1963 ; Heath, 1965 ; Murrish & Vance, 1968 ; Heatwole et al., 1969; Heatwole, 1970; Webb et al., 1972) and indeed has been demonstrated to function in dissipating the heat produced by thermally imposed high metabolic rates, or even to reduce body and/or head temperature (Templeton, 1960; Dawson & Templeton, 1963; Warburg, 1965a; Dewitt, 1967; Crawford & Kampe, 1970; Case, 1972; Crawford, 1972; Webb et al., 1972); in other species that ventilate during mouth-opening, or even in the same species under other conditions, thermoregulatory function is less pronounced (War-burg, 1965b; Dawson & Templeton, 1966; Crawford & Kampe, 1971).

ALTHOUGH

799

Species

No

Gekkonidae Chondrodactylus

angulifer

Aguidae Gerrhonotus multicarinatusf

Uromastix acantherinus

No

36.5 (324-39.0)

38

-

-

-

About 39

-

-

-

No

No

Physignathus lesueueri

No

No

D. bilineata *

No

No

Diporiphora bilineata*

No

No

No

No

kingii

Chlamydosaurus

No No

No No

40.4 (38.2-41.8) 34.8

No No

A. muricatus A. pictus

No

No

No

31.3, 38.4

No

A. inermis

No

-

No

-

No acclimation, solar

No acclimation, non-radiant

No acclimation, solar No acclimation, radiant Acclimation 31-32”C, dark Variable No acclimation, radiant No acclimation, radiant Acclimation 2O”C, radiant No acclimation radiant Acclimation 20°C radiant No acclimation, radiant

13

Stebbins (1961)

Dawson & Templeton (1966)

Langlois (1902)

N=l

N=7

N=2

This paper Johnson (unpublished data) N=l

Heatwole (1970)

N=

Cowles (1956)

-

THEYOCCUR

Authority

(TB) AT WHICH

Acclimation and heating conditions

THE THRESHOLDS

Gular Gular Flutterpumping ing

BYREPTILESAND

No

38.0 (315-42.2) 44.1 (40.8-46.7) See text 39.9 (39+41*2) 30.9

No

39.6, 37.8

Panting

Amphibolurus barbatus

Gaping

RESPONSES TO HEATINGEXHIBITED

mouth opening

I---TYPES OF MOUTH-OPENING

Agamidae Agama atricollis

Lizards

TABLE

8

z %

0

z?

*+I For ex&nation

Iguanidae Anolis acutus

Underwoodisaurus milii

Phoptropus after

P. garrulus

Ptenopus carpi

Palmatogecko rangei

P. cape&s

see

P.

806.

No

0. tryoni

No

No

No

0. sp.

X(a)

No

0. marmorata

bibroni

No

0.1. rhombifer

Pachydactylus

No

0.1. lesueuri

36.9 (36.2-37.7)

42.0 (41.4-42.5) 38.3 (36.7-40*1)

36.2 (32.0-37.7) 34.8 (31.0-38.2) 37.4 (b) (35.0-39.7)

37.0 (36.k37.5) 35.2 (334-36.8) 38.2 (37.3-39.3) 37.8

39.3

No

Oedura coggeri

38.8 (36.0-41.0) 37.5 (346-40*3) 37.5 (33.8-39.9) 36.3 (33.8-IO.S) 39.0,41*6

No No

vittatus

Gehyra variegata

Diplodactylus

No

No

-

-

-

-

No

No

-

No

No

No

No

No

No

Yes

-

-

Yes

Yes

-

Yes

Yes

Yes

Yes

Yes

Acclimation 3O”C, non-radiant

Acclimation 2O”C, radiant Acclimation 2O”C, radiant Acclimation 2O”C, radiant Acclimation 2O”C, radiant Acclimation 2O”C, radiant Acclimation 33”C, non-radiant No acclimation, radiant Acclimation 2O”C, radiant No acclimation, solar No acclimation, solar No acclimation, artificial heat No acclimation, artificial heat No acclimation, solar (a) Artificial heat (b) No acclimation, artificial heat Acclimation 2O”C, radiant N=4

Webb et al. (1972)

Brain (1962)

Stebbins (1961a) Brain (1962b)

Brain (1962)

Brain (1962)

Stebbins (1961)

Stebbins (1961)

N=9

N=2

N=l

N=2

Webb et al. (1972)

N=7

N=8

N = 4

P. solare

P. platyrhinos

-

-

-

42.8 (41443.9) 43.2 (41.7-44.6) 44.1 (425-45.0) 40.3

Phrynosoma cornutum

P. coronatum

-

about 42

-

No

-

-

-

-

No

-

No

No

No No

No

No

Iguana iguana

(32.8-39.4) 36.2 39.7 (37.0-41.8) (425-43.0)

(2&S-32+3) 30.3 39.2 (364-43.5) 39.3 (37%41*0) 39.4 (38441~0)

Panting

AND

THE

No acclimation, non-radiant No acclimation, solar No acclimation, radiant No acclimation, radiant No acclimation, radiant No acclimation, radiant

g ,m F

Heatwole et al. (1969) Heatwole et al. (1969)

Heath (1965)

Heath (1965)

Heath (1965)

McGinnis & Brown (1966) Heath (1965)

Dawson & Templeton (1963), Templeton & Dawson (1963) Templeton (1960)

Heatwole et a1.(1969)

Ruibal(l961)

3 m

5

2

F g

!z a

9 v ; 2

2

5

Ruibal(l961) Heatwole et al. (1969)

B

F 9 b z

(TB)

Authority

THRESHOLDS

No acclimation, solar Acclimation 30°C non-radiant Acclimation 3O”C, non-radiant Acclimation 30°C non-radiant No acclimation, solar Acclimation 30°C non-radiant No acclimation, non-radiant

Acclimation and heating conditions

BYREPTILES

Gular Gular Fluttering pumping

THEYOCCUR

TO HEATINGEXHIBITED

-

Gaping

AT WHICH

RESPONSES

(43-44)

collaris

No mouth opening

OF MOUTH-OPENING

One individual

(cont.)---TYPES

Dipsosaurus dorsalis

Crotaphytus

A. stratulus

A. homolechis

A. gundlachi

A. ewermanni

A. cristatellus

A. allogus

Species

TABLE 1

occidentalis

No

39.0

No No

No No

X

X

E. Cunningham

E. hosmeri

*t$ For explanation see p. 806.

No

No

X

Egermk bungana

Ctetwtus pantherinw

No

44.1

Scincidae Carlia fusca

No

40.8 (406-41*1) 43.4

42.2 (41.0-42.9) 43.1 (41+44*1) 40.7 (395-41*6)

36.0

No

approx. 34-s-39.5 about42

Pygopodidae Pygopus nigriceps

Scaptira suborbitalis

M. suborbitalis

Meroles cuneirostris

Eremias lineo-ocellata

Lacertidae Aporosaura anchietae

utameatk

Scekqwus

Sauromalus obesus

No

No

No

No

No

No

No

No

No

No

-

-

-

-

-

No

No

-

-

-

-

-

-

-

-

-

Acclimation 2O”C, radiant No acclimation, non-radiant Acclimation 35°C radiant No acclimation, radiant Acclimation 2O”C, radiant

No acclimation, radiant

No acclimation, artificial heat No acclimation, solar No acclimation, artificial heat No acclimation, artificial heat No acclimation,

No acclimation, non-radiant various, non-radiant Various, non-radiant

Johnson, unpublished data Webb et al. (1972)

N=l

N=l

N=l

Johnson, unpublished data

Stebbins (1961)

Brain (1962)

Brain (1962)

Stebbins (1961)

Brain (1962)

Crawford& Kampe (1970) Case (1972) Lashbrook & Livezey (1970) Murrish & Vance (1968)

--

Species No

Gaping

(39-2-42+2)

fizards

One 36-4 individual 41.2 Two individuals (40.1-42~U)

fizarcts

Four Three individuals individuals 72% of 28 7; of

No No

No

No

No NO

No

No

NQ

No

No

No

No

NO

individuat 43.2

Na

l-a

No

No

one

T-WC3

individuals

No

No

Na

Na

No

NO

NC%

No

NO

No

No

No

NQ

X

No

Na

No No

No

NO

NC3

No

Panting

Gular G&r Flutterpumping ing

41.7 (41~0-43Q No

Three FOUE individuals individualis X No

43-7 Two individuals (43.2-448) X No

x

No

mouth opening __ -

Acclimation 30°C, non-radiant Acclimation, variable non-radiant

No

acc~at~o~, radiant Acdimation 33”C, non-radiant No acclimation, radiant Acclimation 20”C, non-radiant

SOhI-

Accl~atiQn 35”6, radiant Acdimation, variabk non-radiant No acclimation, non-radiant No acclimation, radiant No ac&mation, radiant Acclimation 2O”C, non-radiant No acclimation,

Acclimation and heating conditions

N=

N=2 14

2 D

Veron & Heatwole (1970)

2

N=7

i

F $ tt

$ 5 Q

N=l

W=?

N=l

Authority

rugosa f

X

X

*t$ For explanation see p. 806.

Notechis scutatus

No

No No

No

X

Elapidae Cryptophis nigrescens

No

About 41

No

No

Colubridae Salvadora hexalepis

Morelia spilo tes

Boidae Liasis childreni 28.8

No

No

Varanus spp.

Snakes

No

No

About 39

Varanidae Varanm aremrius

Varanus gouldii

45

About 37.5 40.5

Teiidae Ameiva exsul

T. scincoidesf

T&qua

No

No

-

No

No

35-8, 40.1 About 38

-

No

No

-

No

No

No

No

-

-

No

No

-

-

-

Acclimation 32”C, non-radiant No acclimation, radiant

Acclimation 27”C, radiant

No acclimation, radiant No acclimation, radiant

No acclimation, radiant No acclimation, solar No acclimation, non-radiant

Acclimation 3O”C, non-radiant

No acclimation, non-radiant No acclimation, radiant

N=l

N=l

Jacobson & Whitford (1971)

Johnson (in preparation) N=l

Bartholomew & Tucker (1964)

Johnson (1972)

Langlois (1902)

Heatwole et al. (1969)

N=l

Warburg (1965a)

g

WI

AND FOOTNOTES

TO TABLE

1.

Dashes indicate data unavailable. Some “panting” thresholds from the literature may actually be “gaping” ones; when category uncertain, values are listed in the panting column with the gaping one left blank. Single numbers are means, multiple ones are individual measurements, and those in parentheses represent ranges. X means that the type of response has been observed but that temperature measurements were not made. No means the type of response does not occur. When no authority is listed, the data are the authors’ previously unpublished results, in which case the number of individuals tested (N) appears in the authority column. * Bradshaw and Main (1968) give field TB much greater than these panting thresholds. The low values in this table may have resulted from the low acclimation temperature. An alternative is that D. australis (the form listed in this table) is taxonomically distinct from D. bilineatu and should not have been synonomized with it as was done by Glauert (1961). + Panting is discontinous. 1 May include values based on defensive mouth-opening.

NOTE

PANTING THRESHOLDS OF LIZARD&I

807

Gular movements occur throughout a wide range of temperature in some lizards and presumably have a respiratory function. In some geckos the rate at which this occurs increases with increasing temperature, and during heat stress may reach such a high frequency as to resemble avian thermoregulatory gular fluttering; it probably increases the effectiveness of panting. The increase in frequency is most marked at initiation of panting and corresponds with a reduction in head temperature (Webb et al., 1972). In some varanids, there is a marked increase in amplitude of gular movements which Bartholomew & Tucker (1964) considered the functional equivalent of panting. Pumping occurred at a rate of about 1 per set and did not reach a sufficiently high frequency to be designated as fluttering. To standardize terminology, the first category of response to high body temperatures (mouth opening following reduction in ventilation; no thermoregulatory function) will be called “thermal gaping”, the second one (mouth opening during high ventilation rates and functioning in evaporative cooling) will be known as “panting”; high amplitude gular movements will be called “gular pumping” and high frequency ones “gular fluttering”. The last may occur simultaneously with panting. The temperatures at which the first two responses are initiated can be respectively called the “gaping threshold” and “panting threshold”. The temperature at which rate of gular movements increases abruptly is termed the “threshold of gular fluttering” and that at which they show a marked increase in amplitude can be known as the “threshold of gular pumping”. The present paper (1) demonstrates that Amphibolurus muricutus (family Agamidae) pants but does not exhibit pronounced gular pumping or gular fluttering, (2) deals with some of the factors influencing the panting threshold and (3) reviews previous work on reptilian panting thresholds. One of the aims of the series of papers of which this is the first, is to assess the influence of photoperiod and thermal acclimation on the panting threshold. During studies in which animals were confined under specific conditions prior to measurement of their panting thresholds, replicate series were opportunistically run, or observations made which permitted evaluation of the role of size, random variation, method and rate of heating, genetic differences, sex and multiple testing as determinants of the panting threshold. These topics form the basis of the present paper. Although different seasons, photoperiods and acclimation temperatures are involved in the experiments reported here, they are incidental to the present discussion and the effects of these variables will be treated in detail in a future paper when additional information becomes available.

GENERAL THERMAL ECOLOGY OF A. muricatus Compared to a number of other species in the genus, A. muricatus occupies a relatively cool habitat. It is found in savannahs, open woodlands and roadsides in the coastal areas and plateaux of eastern New South Wales and Victoria, Australia,

28

808

HAROLDHEATWOLE, BRUCET. FIRTH AND GFUHAME J. W. WEBB

an area with a south-temperate climate. It does not extend westward onto the hotter, arid plains (Witten, 1972). Using a YSI Telethermometer, core body temperatures of thirty-eight animals in the field were measured by inserting a thermistor probe into the intestine via the cloaca. One animal in the process of morning emergence had a body temperature (T,) of 20~9°C. Three were found under logs or stones during their inactive periods; these had a mean TB of 27.5”C (range 23-l-34*2”C). The remainder were taken during their activity period ; thirty-two captured on sunny days had a mean TB of 34%‘C (range 29-S-38*6”C, standard error 0*34”C), whereas two taken on overcast days had TBs of 26.9 and 28GS”C respectively. The activity of twenty-four of those captured on sunny days was noted. Mean TB of fourteen which were corresponding values for ten perched, but basking was 33.6”C (range 30+35*1”C); non-basking, individuals was 34GF’C (range 29*5-38~6°C). We have observed this species employing the thermoregulatory devices of basking, flattening and changing angle of orientation to the sun described for other members of the genus (Bradshaw

MO: (b)

-50

220-

0

4

6

IL I6 20 24 26 22 S6 40 44 46 62 66 60 64 66 72 76 6064

66 92 26

Time, min FIG. 1. Effect of slow radiant heating on body temperature, heart rate (a) and breathing rate (b) of two A. muricutus. Black bars indicate time the lizards were active. L signifies large breaths, M medium ones and S small ones. HR, heart rate; BR, breathing rate.

PANTING THRESHOLDS OF LIZARDS-I

809

&

Main, 1968; Heatwole, 1970; Brattstrom, 1971). Spellerberg (1972) lists this species as a “posturing heliotherm”. Sixteen animals previously kept for 7-12 days in darkness at 20 f 1~5°C were separately studied in a substrate temperature gradient with a range from 0.5 to 50°C (apparatus described by Veron & Heatwole, 1970). Uniform overhead fluorescent lighting was provided. Each lizard had a YSI cloacal thermistor with the lead taped to the tail; periodic readings at intervals of at least 1 hr were made with a YSI telethermometer. The mean of 110 such records was 34~6°C (range 24*5-+2*4”C, standard error 0.56”C). Licht et al. (1966) using a photothermal (radiant) gradient obtained similar results for A. muricatus (mean body temperature 36*O”C, standard deviation 1_22”C, range 32*9-38*6”C, N = 6). Thus mean body temperatures measured on active animals in the field, in a substrate gradient and in a photothermal gradient were similar (34*8,34.6 and 36*O”C,respectively). The mean critical thermal minimum (loss of righting response) of two animals caught in the field in summer was 3mO”C(range 2*5-3.5”C); acclimation at 2~0°C lowered it to near 0°C (Spellerberg, 1972). The mean critical thermal maximum (again loss of righting response) of summer animals from the field was 42~3°C (range 42*1-42*4”C, N = 2) (Spellerberg, 1972). The latter determination involved a radiant heat source. Five animals heated with a non-radiant heat source (see methods of Veron & Heatwole 1970) exhibited spasms at a mean TB of 43vO”Cand had ceased all movements, including respiratory ones, at a mean TB of 43.6”C. Two animals were radiantly heated very slowly (0*2_0*3”C/min); they did not display spasms until TB exceeded 47°C (Fig. 1).

MATERIALS

AND METHODS

All animals but one (used in the experiment on heart rate) were captured in the vicinity of Armidale, N.S.W. Heating and temperature measurement All measurements of panting threshold were made between the hours of 0900 and 1700. Two methods of heating were employed. One involved radiant heat and the other heating in a water-bath. For the former, each lizard was placed in a moulded glass terrarium (32 cm long, 18 cm wide, 20 cm high) provided with a Styrofoam floor (2 cm thick). The animal was immobilized by taping its legs to the Styrofoam with masking tape. Core temperature of the body was monitored by either thermistor probes (YSI or Grant) or thermocouples inserted approximately one-third of the body length into the intestine via the cloaca. Readings were taken at minute intervals with either a YSI telethermometer, a Grant Multipoint Recorder or a Comark Electronic Thermometer (readability 0.2, 0.2 and O*OS”C respectively); all were calibrated against a Negretti and Zambra standard thermometer. The leads were secured by taping to the base of the tail with masking tape. Radiant heat was applied by a 275-W infrared lamp. Preliminary experiments indicated that centering the light 47.5 cm above the lizard’s back resulted in a mean heating rate of approximately lV/min (actual values varied somewhat, see Table 6). This rate was always used except in (a) experiments testing the effect of varying heating rate and (b) one experiment in which two animals were heated slowly in order to ascertain type of response. This method will subsequently be referred to as heating under standard conditions.

810

HAROLDHEATWOLE,BRUCE T. FIRTH AND GRAHAMEJ. W. WEBB

The second method of heating was a modification of that described by Heatwole et al. (1969) and Veron & Heatwole (1970). Lizards with thermistor probes in the intestine were placed in an 1800-ml beaker equipped with a Styrofoam floor 2 cm thick. The container was closed with a Styrofoam top containing a hole for passage of thermistor leads and for air exchange. This apparatus was submerged nearly to the brim in a water-bath which was then intermittently heated by a Bunsen burner so that the animal heated at about l”C/min. The water was stirred by the action of an aquarium air bubbler. Air temperature was monitored by thermistors suspended at the lizard’s mid-body height. This will subsequently be referred to as “non-radiant” heating. In all experiments, temperatures were read at minute intervals, at the voluntary maximum (see below) and at the onset of panting. In some experiments head temperatures were also measured at the panting threshold. This was achieved by inserting a hypodermic thermistor probe deep into the posterior head musculature just posteriolateral to the base of the skull. Acclimation

conditions

Panting thresholds were measured on (a) field-caught animals on the day of capture, and on (b) those previously confined under specific, controlled environments for 7-12 days in cages with water but no food. Animals used in more than one experiment were fed between acclimation periods. Specific photoperiods and temperatures used during acclimation are indicated in the appropriate results sections. However, the effect of photoperiod and thermal acclimation are discussed in a later paper. Breathing rate In some experiments, the number of breaths counted for the first 30 set of each minute, were used to calculate breathing rate. A. muricatus suspended various activities, including breathing, when disturbed. In the present study, periods of apnea occurred in response to someone entering the room or to conspicuous movements by the investigator. Counts including such periods were discarded. As tidal volume contributes to ventilation and no means of quantitative measurement of it was available, breaths in each counting period were qualitatively categorized as small, medium or large. Voluntary maximum The highest temperature a lizard will voluntarily accept without attempting to escape is the voluntary maximum. In the present study, animals usually remained quiescent during heating until high temperatures were reached. They would then suddenly struggle violently against the restraining tapes. Body temperature at which such activity was initiated was considered to be the voluntary maximum. RESULTS

Type of response Two individuals were radiantly heated at a slow rate (0.Z0*3”C/min) until dead in order to ascertain which, if any, of the several types of responses to high temperature was exhibited. One non-acclimated animal had its heart rate continuously monitored (by a Both recorder with a Tektronix FM122 low level pre-amplifier). A second one (acclimated at 25°C in a photoperiod of 8L 16D for 1 week) had breathing rate counted. In both, core body temperatures and all activity were noted. Both ventilatory and circulatory function extended well beyond the time the mouth was first opened (Fig. 1). Consequently the avenues of evaporative cooling and of heat transport within the body are intact at this time. At the very low

PANTING

811

THRESHOLDS OF LIZARDS-1

heating rates employed in this experiment, the time between panting and the first sign of heat damage (spasms or cessation of breathing) was 284 min. Panting threshold in the first animal was 40.9”C and spasms did not occur until 47*3”C, a range of 6.4 centigrade deg in which panting could be of survival value. The second animal panted at 42WC and ceased breathing at 47*1”C, a span of 4.3 centigrade deg. Five of the animals of the non-radiant heating series (see below) were heated above the panting threshold until dead. The mean panting threshold was 39qO”C and the first sign of heat damage (spasms) did not occur until a mean TB of 43.O”C. During the 4 degree span in which panting occurred, breathing rates were among the highest values obtained (Fig. 2); considering that tidal volume was also observed to be elevated at this time, ventilation was at a maximum.

-I6

-14

-12 Time

FIG.

-10 beforeand

-6

-6

-4

-2

after onset of panting,

0

2

4

min

2. Mean breathing rates of five non-radiantly heated A. muricatus, previously acclimated for 1 week at 20°C in constant dark.

Except for the above runs, all experiments were stopped as soon as the mouth was opened. However, runs in which breathing rates were counted provided some data relevant to the type of response involved. Initially, breaths of large volume were most prevalent, presumably in response to the lizard having been handled. After 7-8 min, frequencies of all three categories of tidal volume were nearly equal. However, as the panting threshold was approached, the proportion of large breaths increased greatly, with the proportion of others (especially small ones) decreasing accordingly. In addition, regardless of the category of breath size employed, the rate progressively increased until the onset of panting (Fig. 3). Thus, both components of ventilation increased in the pre-panting period. All of the above observations converge to indicate that A. mwicatus exhibits true panting and not merely thermal gaping. However, quantification of the effectiveness of panting as a means of dissipating heat in this species must await studies of water loss under various environmental temperatures and saturation deficits.

812

HAROLD

HEATWOLE.

0

l-r

2

BRUCE T.

I 4

I

6

I

6

FIRTH AND GRAHAME

I

I

I

I

I

r

I

J. W.

WEBB

II

10 I2 14 I6 16 20 22 24 26

Minutes priortothe onset of ponting

Change in proportion (a) and frequency (b) of small, medium and large breaths during heating of A. muricutus. In part (b), each point represents the mean of from ten to eighty values, depending on the number of animals employing a given type of breath for the time period under consideration. Lines fitted by least squares methods. Other symbols as in Fig. 1. FIG. 3.

Effect of body size

If age and/or body size influence panting threshold, two samples subjected to different treatments could not be validly compared if their size structures were different. Consequently, for each sample in which body length was measured, a regression analysis of panting threshold vs. snout to vent length was performed. In no case was the slope of the regression line significantly different from zero (ttest, see Table 2). It can be concluded that in this species, and for a given treatment, panting threshold does not vary with body size. Eflect of sex

Females are much less frequently encountered in the field than males. Whether this is because of a skewed sex ratio, or because females are better camouflaged or differ from males in microhabitat or behavioral patterns, is unknown. It did, however, result in our samples consisting almost entirely of males and a sample of females large enough for statistical comparison with males was seldom obtained. Females usually had a lower panting threshold than males (Table 3). In the single

PANTING

THRESHOLDS OF LIZARDS-I

TABLE 2-%EZJLTS OF REGIIESSION ANALYSISOF PANTING

813

THRESHOLD

vs. SNOUT

To VJBIT

LENGTH

Acclimation temperature (“C), photoperiod and site of temperature measurement Field-caught, Field-caught, Field-caught, Field-caught, Field-caught, Field-caught, Field-caught,

7 Oct., 1970, TB 7 Oct., 1970, TH 8 Oct., 1970, TB 8 Oct., 1970, TH < 9 Oct., 1970, TB 9 Oct., 1970,TH 22 Feb.-2 March, 1971,

Slope of regression line

> 0.50 0.40 > P> 0.20 > 0.50 >o*so O*lO> P>O*OS > 0.50 0*20>P>0*10

89-123 89-123 91-118 91-118 88-126 88-126 86-119

t

< O*OOl 0.031 < owl - 0@01 - 0.064 - 0.009 0.083

0.03 1 moo < 0.01
0.030 0.114

0.83 1.16

0*50>P>04 040>P>0*20

78-119 77-l 27

0.039

0.51

> O-50

77-l 27

>0*.50 > 0.50 > 0.50 0~10>P>0*05 0~50>P>040

95-126 73-l 24 80-111 76-l 11 97-123

TB

2O”C, dark, Tn 2O”C, constanilight, double heating rate, TB 2O”C, constant light, double heating rate, TH 25”C!, 16L 8D, Tn 2X?, 8L 16D, T; 6°C (dark 16 hr), 26°C (light 8 hr), TB 27’C, constant light, TB 26”C, constant light, TS

P

Range in s-v length b-d

0448 - 0.376 0.810 - 3.760 - 2.508

0.36 0.057 3.82 2.30 0.75

TB indicates core body temperature at the panting threshold; TE indicates head temperature. TABLE 3-COMPARISON OF PANTINGTHRESHOLDS OF MALESAND FEMALES OF A. Males Treatment

??UiYiCUtUS

Females

N

Mean

9 9

40.8 40.9

; 9

37.3 39.9 39.1

TH TB Acclimated 25°C in light, Oct. 1970

9 9

41.2 42.1

1 1

40.5 41.2

TE TB Acclimated 2!Y’C, 8L 16D

9 9

40.7 41.0

1 1

40‘0 39.8

1

40.8

1

42.2

iv

Mean

Field-caught, 7 Oct., 1970, TH TI3 Field-caught, 11 Acclimated 20°C Acclimated 20°C Acclimated 25°C

March, 1971, in dark, Dec. in dark, Nov. in dark, Oct.

TB 1971, TB 1971, TB 1970,

TB l

Omitting a shedding individual.

39.9 40.3 37.6* 36.9 36.7

814

HAROLDHEATWOLE,BRUCET. FIRTH ANDGRAHAMEJ. W. WEBB

sample which could be tested statistically (20°C dark, Dec. 1971) females did not differ significantly from males (Mann-Whitney U-test, two-tailed, P = O-10). When all means were considered as individual values and paired by treatment and subjected to a Wilcoxon matched-pairs signed-ranks test (two-tailed) the difference between the sexes was not significant when only values of TB were used (P>O*OS) or when those of TB and TH were considered together (P> O-05). It appears that there is no difference in panting threshold between the sexes. However, the rather consistently low values obtained from females and the small sample sizes do not inspire a high measure of confidence in this conclusion. Consequently, in all other analyses only data from males were used unless otherwise specified. Effect of shedding Two samples contained lizards which were in advanced stages of shedding the skin. They appeared white and had almost the entire outer layer of the skin loosened and flaking off. In both samples, shedding lizards had a slightly higher mean panting threshold than those not ecdysing. However, in the single sample (25°C 8L 16D) with sufficient individuals to test statistically (N = 8, 3), the difference between the shedding and non-shedding lizards was not significant (Mann-Whitney U-test, two-tailed, P = 0.496) (Table 4). In no other sample was there such a high incidence of shedding although an occasional individual had remnants of loose skin evidencing recent ecdysis. TABLE ~-COMPARISON OF PANTINGTHRESHOLDS (TB) OF SHEDDINGAND NON-SHEDDING A. muricatus Non-shedding Treatment Field-caught, * March 1971 Acclimated 25”C, SL 16D

Shedding

N

Mean

N

Mean

4 8

37.6 39.4

1 3

38.6 40.2

* All females, a single male eliminated from the analysis.

It appears that the shedding cycle does not influence the panting threshold. However, because of the small sample size used in the analysis, data from shedding animals were eliminated from all other analyses. Effect of repeated determination

of panting

threshold

Short-term effects. A male individual (34.7 g) was kept for 3 weeks at 15-25°C in constant darkness (except for brief periods when someone entered the chamber to take out other lizards). Its panting threshold and voluntary maximum were tested under radiant heat. Body temperature was raised from 24~8°C until the animal panted. The lamp was then turned off and the animal permitted to cool several degrees below the panting threshold. The lamp was then turned on again

815

PANTING THRESHOLDS OF LIZARDS-I

and this process repeated until ten consecutive, regularly spaced tests had been carried out over a period of 3 hr and 10 min. During these tests the lizard lost 0.8 g (2.3 per cent of original body weight). At least some of this weight loss was urine voided when the thermistor was removed at the end of the experiment and thus evaporative loss must have been very slight. As the vital limit of water loss in lizards usually exceeds 20 per cent (see Sexton & Heatwole, 1968), it is unlikely the animal was in moisture stress. An attempt was made to ascertain body temperature at which panting ceased during cooling periods between tests. This was not possible because the lizard gradually closed its mouth and no sharp end-point could be detected. However, the mouth was kept widely open at temperatures lower than that at which panting was initiated during heating. There was a statistically significant lowering of the panting threshold with consecutive testing (Spearman rank correlation test, two-tailed, Y, = - 0.97, P-c O-02) (Fig. 4); thus, exposures to high temperature results in earlier initiation of thermoregulatory panting on subsequent exposures. The decrease was gradual

I IfI

12345616

” Test

”

”

9

’ IO

I

number

4. Effect of repeated heating at short intervals on the panting threshold (dots) and voluntary maximum ( x ‘s) and TmT, (circles) of A. muricutus. TprTvM signifies the difference in body temperature between the panting threshold and the voluntary maximum.

FIG.

at the beginning, with the greatest drop between the last two tests, suggesting an increase in the rate of adjustment with continued frequent exposure to high temperatures. The difference between the largest and smallest values was 1.3 centigrade deg. (mean decrease of 0.41 deg./hr or 0.14 deg./test). Whether these short-term adjustments represent physiological acclimation or temporary behavioral changes (perhaps learning) awaits further experimentation. The voluntary maximum was more variable than the panting threshold but showed an even greater decrease with repeated heating (Fig. 4) (Spearman rank correlation test, two-tailed, Y, = - 0.84, P-e O-02). The first value was not recorded because of technical difIiculties but of the nine others, the difference between

816

HAROLD HEATWOLE, BRUCE T. FIRTH AND GRAHAME J. W. WEBB

highest and lowest was 36 centigrade deg., a mean decrease of 1.14 deg./hr or 0.45 deg./test. The more rapid decrease in voluntary maximum than in panting threshold resulted in a progressively (and significantly) greater thermal margin between these test, two-tailed, rs = O-60, two end-points (Fig. 4) (Sp earman rank correlation P-C 0.05). Thus, with frequent exposures to high temperatures these lizards initiate escape from heating environments at progressively lower thermal levels. This is reminiscent of the downward shift in preferred temperature of Sceloporus occidentalis when acclimated at high temperatures (Wilhoft & Anderson, 1960). Long-term efects. The previous experiment elucidated changes in panting threshold caused by experiencing high temperatures a number of times in rapid The present one examines the effect of being subjected to panting once succession. of 8L 16D, each day. A male (54.8 g) acclimated at 25°C for 1 week at a photoperiod was radiantly heated each day between 1000 and 1100 hr. It was kept under the acclimation conditions during the 9-day test period except when actually being tested. It appeared healthy after the test of the ninth day but was dead the following It is unknown whether this was a result of periodically imposed heat morning. stress or of some other factor. The lizard’s panting threshold fluctuated widely from day to day but showed no consistent trend with time (Fig. 5); correlation of panting threshold with test 427 4140-

< 39 .o

:

39-

’

k

LL 3736

/-

i

1’

I

\

i \ 1 \ ‘Lx

i 1 \ / ’ I’ k

0 x

35 341 Field caught

I

I

I

I

I

I

I

I

I

123456789

Test day

FIG. 5. Effect of repeated heating at day intervals on the panting threshold (dots) and voluntary maximum ( x ‘s) of A. muricutus. One week’s acclimation occurred between measurements on the field-caught animal and test day No. 1.

number (time) was not significant (Spearman rank correlation test, two-tailed, r, = -0.23, P> 0.10). On the basis of this experiment and the previous one it seems that (1) on a given day the panting threshold remains at a nearly constant level, decreasing slightly with increasing number of exposures to high temperature,

817

PANTINGTHREEHOLDSOFLIZAF(DS-I

but that (2) rather large day to day fluctuations occur which are of much greater magnitude than the total range of ten consecutive trials on a given day. Any effect that heating has upon panting threshold on the following day, if present at all, is small enough to be completely masked by the normal day to day variation within an individual. The voluntary maximum also varied from one day to the next; it followed the same pattern as the panting threshold but was more variable. There was no correlation of voluntary maximum with test number and thus no effect of multiple exposure was demonstrated (Spearman rank correlation test, two-tailed, rs = - 0.47, P> 0.10). Eflect of intra-population genetic dajkrences. One would expect that within a population there would be individuals genetically disposed toward higher panting thresholds than others. If certain animalstend to have consistently higher thresholds, and if the same group of individuals is used for several determinations, there should be a correlation of the relative performance of individuals in different tests. This did not prove to be the case as panting thresholds of lizards subjected to one treatment, plotted against their own values obtained under another treatment, resulted in a wide scatter of points in each case. High scorers in one trial did not have a consistent tendency to score high on other ones (Spearman rank correlation test, see Table 5) and thus no consistent individual differences were demonstrated. Day-to-day variation in panting threshold within individuals may have been great enough to obscure small differences among individuals. TABLE

S-RESULTS

OF CORRELATION ANALYSIS OF PANTING THRESHOLDS ONETl3STWITHVALUFSOBTAINED ON ASUBSEQUENTONE

Acclimation treaments Field-caught Field-caught 25°C in light Field-caught Field-caught 30°C in light Field-caught

vs. 25°C in light vs. 25°C in dark vs. 25°C in dark vs. 30°C in light vs. 10°C in dark vs. 10°C in dark vs. 5°C in light

N

YE

9 8 8 10 10 10 10

0.22 - 0.14 0.34 0.47 0.43 0.37 0.26

(TB) OBTAINED

ON

P > > > > > > >

0.05 0.05 0.05 0.05 0.05 0.05 0.05

The two scores for each individual were plotted against each other. Spearrnan rank correlation test, two-tailed. Both sexes are included.

All the above lizards came from the same locality. Genetic differences among populations from different localities remain to be tested. Head-body temperature da~erences at the pant&g threshold. If, as has been suggested (Heatwole, 1970), head temperature (Z’n) is of more significance in determining panting than is TB, assessment of body temperature alone could give misleading results. Consequently we measured both head and body temperatures at the panting threshold in a number of lizards heated under standard conditions.

818

HAROLDHEATWOLE,BRUCET. FIRTH ANDGRAHAMEJ. W. WEBB

The maximum difference observed between head and body was 3.2 centigrade deg. ; this was exceptional as most values were of less than 1 deg. In five groups of eight to ten animals each, mean Tu minus mean T, at the panting threshold was 0.3, - 0.4, - 0.2, 0.1 and - O-2 centigrade deg., respectively (Fig. 6). In no group were the differences between the means for head and body significant (Wilcoxon matched-pairs signed-ranks test, two-tailed, 5 per cent rejection level). Similarly, thirty field-caught animals had a mean TB of 40*8”C and a mean TH of 40*5”C at the panting threshold (difference between the two not quite significant; P = 0.0526, Wilcoxon matched-pairs signed-ranks test, two-tailed) (Fig. 6).

46r(d

44 42 40 oc 38 36 34 32 30

FIG. 6. Comparison of head and body temperatures at the panting threshold of A. muricutus. Open figures represent TB, black figures TH. Vertical lines represent the range, central horizontal lines the means and rectangles two standard errors on each side of the mean. Failure of rectangles to overlap indicates a significant difference between means (approx. rejection level of 5 per cent) (Dice & Leraas, 1936). (a). Twenty-nine animals field-caught, 7-9 Oct., 1971 and tested immediately at standard radiant heating rate. (b). Animals tested at standard radiant heating rate after acclimation at: (1) 5°C in constant light, (2) 10°C in constant dark, (3) 25°C in constant light, (4) 25°C in a photoperiod of 16L 8D, (5) 30°C in constant light. N = 9-10 for each group. (c). Ten animals radiantly heated at double rate after acclimation at 20°C in constant light. Cross-hatched figure represents panting threshold (TB) of nine animals acclimated in constant light and radiantly heated at standard rate.

In none of the above groups was mean TH - TB significantly different from zero (Dice-Leraas Graphic Test, approximately 5 per cent rejection level) (Fig. 7). Thus, at the panting threshold in A. muricatus heated under the conditions of these experiments, the more easily measured TB serves equally as well as TH. This may not be true for A. muricatus in other temperature ranges. In other reptiles there are often significant head-body temperature differences during initial warming, and when approaching tolerance limits (Heath, 1964, 1965; Campbell, 1969; Johnson, 1972; Webb &Johnson, 1972; Webb et al., 1972). and radiant Radiant vs. non-radiant heating. A. muricatus is a heliotherm heating would thus seem to be the most appropriate means of ascertaining panting

PANTING

THRKSHOLDS

OF LIZARDS-1

819

FIG. 7. Comparison of head-body temperature differences (TcZ’n) at the panting threshold of animals subjected to various acclimations and conditions of heating. (1) Double-heating rate, acclimated at 20°C in constant light. All the remaining heated at standard rate (Nos. l-8 radiantly heated; No. 9 non-radiantly heated) after acclimation under the following conditions: (2) Field-caught, (3) 25°C in 16L 8D, (4) 30°C in constant light, (5) 25°C in constant light, (6) 5°C in constant light, (7) 10°C in constant dark, (8) 25°C in constant dark and (9) 20°C in constant dark. N = 8-10 except for No. 2 where N = 29 and No. 9 where N = 4.

thresholds. However, non-radiant heating has been employed in some previous investigations of heliothermic species, and it was considered desirable to compare the two methods. Twenty animals were captured and acclimated at 20°C in constant dark. Ten were heated by radiant means and ten by non-radiant ones. The body temperature at the panting threshold was slightly higher with non-radiant than with radiant heating though the difference was not significant (Fig. 8). There was much less variation among radiantly heated individuals than among those subjected to non-radiant heating; the standard error of the latter was more than double that of the former (Fig. 8). Mean air temperature at the panting threshold of non-radiantly heated animals was 4+7X!, i.e. well above TB at the panting threshold of any individual of this species. It was considered possible that in contrast to results from radiant heating (see above), head temperature during non-radiant heating might depart widely from body temperature and more closely approach that of the air. If head temperature were the real determinant of panting in both types of heating, true differences in panting thresholds between radiant and non-radiant heating would be obscured by using measurements based on body temperature.

820

HAROLDHEATWOLE,BRUCET. FIRTH ANDGRAHAMEJ. W. WEBB 36-

44 -

42 -

ac

40-

30 36 -

FIG. 8. Comparisons of panting threshold (TB) of nine radiantly heated (open figure) and ten non-radiantly heated (dark figure) A. muricatus. Acclimation at 20°C in constant dark for both groups. Other symbols as in Fig. 6. The 20°C dark samples of Fig. 7 and 8 are different sets of animals collected at different times.

Head temperatures were measured on four individuals subjected to non-radiant heating; body temperature at the panting threshold was equal to or up to 1.6 centigrade deg. higher than head temperature. Clearly, head temperatures do not tend to follow those of the air during non-radiant heating; rather at the panting threshold, they depart from them more widely than do body temperatures. This contrasts with the close relation of panting and air temperature in non-radiantly heated Amphibolunrs inermis (Heatwole, 1970). In summary, radiant and non-radiant heating provide similar estimates of the panting threshold; the former, however, gives more uniform results and is therefore preferable. Comparison of the relative influence of air temperature on panting thresholds in different species is needed. Effect of heating rate. Nineteen lizards were captured in November 1971 and acclimated at 20°C. Nine were radiantly heated at the standard rate until they panted (actual mean heating rate l*S”C/min). The panting thresholds of the other ten were determined with the heat lamp lowered to give a mean heating rate of 2~6”C/min (double heating rate). The mean TB at the panting threshold in the two series differed by only 0.3 centigrade deg. ; the difference was not significant (Fig. 6). However, the variability in results in the fast-heating group was much greater than in the slow-heating one. The standard error for the former (l-20) was almost twice that of the latter (0.7). Heating rates were not uniform even under standard lamp height and placement of lizards. We considered that a more sensitive test of the relationship between

821

PANTINGTHRESHOLDSOFLIZARDS-I

heating rate and panting threshold might be obtained from analysis of regression. Grouping the standard-heated and double-heated animals together and analyzing regression of panting threshold against heating rate gave a slope of O&38, a value not significantly different from zero (Student’s t-test, t = 1.47, 0.20 > P> O-10). Analysis of the standard-heated and double-heated series separately, gave similar results (t = O-73, 0.50 > P> 0.40 for standard heating; t = 1.95, 0.20 > P> 0.10 for double heating). In addition all the other standard-heated samples were individually subjected to the above type of regression analysis. In twenty-one of the twenty-three such tests there was no significant effect of heating rate (in many cases P exceeded O-50). In the two samples in which the slope was significantly different from zero (Table 6), the type of effect was not consistent; in one the slope was negative and in the other positive. The collective data overwhelmingly indicate that heating rate, TABLE

~-ANALYSIS OF REGRESSION OF PANTING THRESHOLD OF A. muricatus

N

Heating rate (‘C/min) Z (range)

Field, 7 Oct., 1970, TB Field, 7 Oct., 1970, TH Field, 8 Oct., 1970, TB Field, 8 Oct., 1970, Tn Field, 9 Oct., 1970, TB Field, 9 Oct., 1970, TH Field, Feb., 1971, TB 3O”C, light, TB 3O”C, light, TH 25°C light, TB 25X, light, TH 25”C, dark, TB 25”C, dark, TH 25”C, 16L 8D, Nov., 1970,

9 9 10 9 10 10 11 10 10 9 9 9 8 10

1.0 (0.7-l ‘2) 1.0 (0.7-l ‘2) 1 .O (0.6-l ‘3) 1.0 (06-l ‘3) 1.0 (0.8-l ‘2) 1 *O(0.8-l ‘2) 1.4 (l*l-2.0) 0.7 (0.5-1.0) 0.7 (0.5-l -0) 0.9 (0.8-l ‘1) 0.9 (0.8-1.1) 1.3 (0.8-2.6) 1.0 (0.8-l -2) 0.8 (0.6-l -0)

TB 25”C, 16L 8D, Nov., 1970,

9

0.8 (0.6-0,9)

TH 25”C, 16L 8D, Dec., 1971 25”C, 8L 16D, TB 2O”C, light, TB 2O”C, dark, TB lO”C, dark, TB lO”C, dark, TH 5”C, light, TB 5”C, light, TE

8 8 10 9 10 9 10 9

0.8 (06-1.1) 1 *o (O-2-2.2) 1.3 (1.1-1.9) 1 .O (0.9-2.6) 0.9 (0.7-l ‘2) 0.8 (0.7-l ‘2) 1.0 (0.8-l ‘2) 1.0 (0.8-l ‘2)

Treatment

b - 1.62 -3.15 1.17 0.34 6.42 - 1.75 0.92 - 1.99 - 0.38 - 4.34 -5.31 - 2.21 0.05 - 1.70 3.01 0.64 - 1.47 5.26 2.13 - 8.27 - 12.34 - 2.28 2.51

vs. INDIVIDUAL HEATING

RATES

t

P

0.88 1.93 0.34 0.15 2.53 1.82 0.30 0.38 0.13 1.48 0.04 0.09 0.04 0.62

0~5O>P>O40 0~10>P>0~05 P>O*50 P>O*50 0.05>P>O.O2 0*20>P>0~10 P>O*50 P>O*50 P> 0.50 0*20>P>0~10 P>O*50 P>O.50 P>O+50 P>O*50

1 a48

0~20>P>0~10

0.27 1.36 1.66 1.04 1.42 3.39 0.35 0.61

P> 0.50 04O>P>O~20 0*20>P>0~10 040>P>0*20 0~20>P>0*10 0*02>P>0*01 P>O*50 P>O*SO

Student’s t-test; null hypothesis of no difference between slope of the regression line (b) and zero.

822

HAROLD HEATWOLE, BRUCE T. FIRTH

AND

GRAHAME J. W. WEBB

within the ranges employed, does not influence the level of the panting threshold as measured by either Z’n or TB. Certain differences between standard and double heating rates were noted, however. Animals heated at the double rate displayed more marked head-body temperature differences than those heated at standard rates. Mean TH at the panting threshold was 40*2X, or 1.4’22 higher than mean TB (38*8”C) (Fig. 6). The magnitude of the differences between TH and TB at the double rate, although not statistically significant (Dice-Leraas Graphic Test) (Figs. 6 and 7) suggests that in experiments employing rapid heating, measurement of head as well as body The slope of the regression line of panting temperature would be advisable. threshold as measured by TH against heating rate was not significant (t = 0.16, P> 0.50). Many of the lizards subjected to the double heating rate showed heat damage even though the lamp was turned off immediately after onset of panting. Of the fast-heating series, only two of the ten animals survived the experiment in an The other eight exhibited unto-ordinated moveapparently normal condition. ments and loss of the righting reaction when removed from the test chamber; one underwent spasms prior to panting. Of those which were heat-damaged, three recovered by the following day; the other five died within a few hours. None of the animals which were heated at the standard rate displayed any symptoms of heat damage. The fact that animals subjected to rapid heating suffered heat damage at the panting threshold whereas those heated slowly did not, suggests that heat damage depends not only on the absolute temperature but on the rate at which temperature is changing. The high temperature tolerance limits of the two animals heated very slowly in the experiment on heart and breathing rates also support this conclusion.

DISCUSSION

It is clear that in future studies of the panting threshold of A. m~ricatus there are certain variables which can be ignored in experimental design as they do not significantly influence the panting threshold. These are (1) body size, (2) repeated testing of a given individual if at least 1 day elapses between tests and (3) head-body gradiants as long as heating rate is moderate. The method of heating did not significantly influence the level of the panting threshold, although results obtained from heating in a water-bath gave much more variable data than did radiant heating, and the latter method is consequently preferable. Several variables did have a significant effect. Rapid heating resulted in highly variable data and increased the magnitude of head-body differences at the panting threshold, though mean differences between TH and TB were still not significant. Rapid heating rates are thus not advisable, but if employed, both TH and TB should be measured and used in comparisons. Heating rate and site of temperature measurement should always be specified. Repeated testing with short intervals between tests causes a slight lowering of the panting threshold and if the same

PANTING

THRESHOLDS

OF LIZARDS-I

animal is used in several tests, at least a day should be allowed between them.

823

Sex and the phase of the shedding cycle did not have significant effects. However, samples were small and these two aspects should be tested further. The major source of variation in the panting threshold seems to be day to day variation within individuals. If radiant heating at a moderate rate is employed, the variation among the panting thresholds of one individual on ten different days (S.E. 0.332) is as great as that among the panting thresholds of ten similarly acclimated lizards on a given day (S.E. 0.300). On any one day the panting threshold of a particular individual shows very little variation despite temporal changes associated with repeated testing at short intervals (S.E. only O-018). This suggests that the variation within a population is largely a result of the day to day intraindividual variations, the various lizards in the population being out of phase with each other. The factors influencing daily shifts in panting threshold remain to be discovered. The literature on reptilian panting is not extensive; indeed a recent review of vertebrate panting (Richards, 1970) made only brief allusion to reptiles. Phylogenetic and ecologic interpretations are currently hampered by the paucity of data and by the fact that a variety of heating methods and acclimation treatments have been used by different investigators. In addition, panting and gaping have not always been distinguished and consequently some of the “panting thresholds” listed in Table 1 should probably be “gaping thresholds”. However, some generalizations can be made. Panting is absent or weakly developed in ski&. Most of the species do not open the mouth even when heated to lethal limits. Of those which did, most only gaped. Webb et al. (1972) h ave also pointed out the inequivalency of the mouth-opening response between &inks and other lizards, although they referred to both types of response as “panting”. The only skink previously reported to pant (Tdiqua rugosa) does not do so continuously at high temperatures but rather engages in “gulping”. It is less effective in thermoregulating by panting than is a similarsized agamid, Amphibolurus barbatus (Warburg, 1965a). We subjected one male individual of Tdiqua scincoides from the Cape York Peninsula to radiant heating. Initial TB was 30.0°C; breaths were shallow and occurred at a rate of 30/min. Beginning at a TB of 40*5”C it sporadically and briefly opened its mouth a few millimetres (Table l), sometimes accompanied by protrusion of the tongue. By 42.8”C the mouth openings had become regular and wide and occurred during each inhalation; the mouth was closed during exhalation. This could be described as “gulping” and is probably similar to the response of T. rugosa. T. scimxides has a very large lung capacity and during most of panting breaths were extremely deep, ranging from 20 to 28/min until a TB of 43*2”C when they became shallow again. At 43.5”C panting ceased and at 43.7”C breathing stopped. Spasms (CT,,.,,,) occurred at a TB of 43*9”C (TH 46-7”(Z). Panting in Tiliqua differs from that in other lizards by being discontinuous and occurring only during exhalation; it probably represents an independent development of the response in a primitively non-panting family.

824

HAROLD HEATWOLE, BRUCE T. FIRTH AND GRAHAME J. W. WEBB

Other than skinks, the single pygopodid tested and most snakes lacked panting (Table 1); however, more species should be tested. Every species in each of the other families (Agamidae, Anguidae, Gekkonidae, Iguanidae, Lacertidae, Teiidae and Varanidae) panted and/or engaged in gular fluttering or gular pumping, with the possible exception of one iguanid species (see below). Also, in two species which normally pant, individuals were encountered which did not (Table 1). The mean panting threshold does not differ greatly among panting species, and lies between 35 and 40°C for nearly all species and families. Those which were were mostly diurnal forms from deserts and other hot regions higher (4045°C) (e.g. A. inermis, Dipsosaurus dorsalis, Phrynosoma spp., Rhoptropus and all the lacertids listed) although several other species also had high thresholds. Not all desert species had high thresholds. In order to assess the ecological correlates of the panting threshold, it will be necessary to make comparisons within a small taxon (e.g. genus) whose members have different ecologies. Only a few such studies have been carried out. Ruibal (1961) found that Anolis allogus panted at 30°C whereas A. homolechis did not do so until Tn reached 36°C. The former occurs in heavily shaded parts of forest, the latter in clearings, along paths or at forest margins. Brain (1962) pointed out that nocturnal geckos from the Namib Desert had lower panting thresholds than diurnal ones from the same area (various genera involved). Heatwole et al. (1969) found very little difference in the panting thresholds of four species of Anolis from different habitats in Puerto Rico. One species, A. gundlachi, opened the mouth only after the breathing rate had decreased markedly and may have gaped rather than panted. However, at mouth opening its breathing rate was still higher than most of the other species which were still in the elevated breathing phase. Consequently the nature of the response of A. gundlachi is not clear. This species occurs in thermally stable, densely shaded forest. Webb et al. (1972) found that within the gekkonid genus Oedura, a species from hot arid regions of Australia (0. coggeri) had a higher panting threshold than one (0. tryoni) from the cooler tablelands. A third species occurred in both areas; a subspecies from the arid area (0. Zesueurii rhombife) had a higher panting threshold than the tableland form (0. 1. Zesueuri). Heath (1965) found that the panting threshold of the desert Phrynosoma platyrhinos was significantly higher than those of the non-desert species (P. cornutum, P. coronatum) ; P. m’calli (from the desert) did not pant at least up to a temperature of 45°C. It appears that within a taxon, there is often, though not always, a correlation of panting threshold with the thermal characteristics of the habitat and/or with the type of activity cycle. Whether differences among panting taxa reflect merely the ecologies of the species sampled for study, the conditions of acclimation used in different studies, or basic inter-taxon differences in thermal adaptation requires investigation of a greater number of species using comparable techniques. These must take into account experimental variables influencing panting thresholds,

PANTINGTHRESHOLDS OF LIzARDtiI

825

Gular pumping and gular fluttering are much more restricted in their occurrence among reptilian taxa than is panting. To date, the former is known only in varanids and the latter only in geckos (Table 1). Acknowledgements-We are indebted to Elizabeth Cameron, Barbara Saylor and John Veron for assisting in the laboratory; to A. F. O’Farrell, Richard Shine, Roger Seymour, John Parmenter, Geoffrey Witten and George Chong for suggestions and criticism; to David Horton for identification of some of the &inks listed in Table 1; and to Len Zell, Elizabeth Zell, Pam O’Hara, Elizabeth Cherry and Sue Dixon for aid in the preparation of the manuscript. The project was financed privately by the authors and by grants from the Society of the Sigma Xi and the Internal Research Funds of the University of New England.

REFERENCES BARTHOLOMEW G. A. & TUCKERV. A. (1964) S ize, body temperature, thermal conductance, oxygen consumption, and heart rate in Australian varanid lizards. Physiol. 2051. 37, 341-354. BRADSHAW S. D. & MAIN A. R. (1968) Behavioural attitudes and regulation of temperature in Amphibolurus lizards. J. Zool. 154, 193-221. BRAIN C. K. (1962) Observations on the temperature tolerance of lizards in the central Namib Desert, South West Africa. Cimbebasia 4,1-S. BRATTSTROM B. H. (1971) Social and thermoregulatory behavior of the bearded dragon, Amphibolurus barbatus. Copeia 1971,484497. CAMPBELLH. W. (1969) The effects of temperature on the auditory sensitivity of lizards. Physiol. Zoiil. 42, 183-210. CASE T. J . (1972) Thermoregulation and evaporative cooling in the chuckwalla, Sauromalus obesus. Copeia 1972,145-150. COLE L. C. (1943) Experiments on toleration of high temperature in lizards with reference to adaptive coloration. Ecology 24, 94-108. COW R. B. (1956) Notes on natural history of a South African agamid lizard. Herpetologica 12, 297-302. CRAWFORD E. C. JR. (1972) Brain and body temperatures in a panting lizard. Science, Wash. 177, 431-433. CRAWFORDE. C., JR. & KAMPE G. (1970) Response of the lizard, SaummaZus obesus to increasing ambient temperatures. Fedn Proc. Fedn Am. Sots exp. Biol. 29, abstract No. 1546. CRAWFORDE. C., JR. & KAMPE G. (1971) Physiological responses of the lizard Suuromalus obesus to changes in ambient temperature. Am.J. Physiol. 220,1256-1260. DAWSONW. R. (1960) Physiological responses to temperature in the lizard Eumeces obsoletus. Physiol. Zoiil. 33,87-103. DAWSONW. R. & TEMPLETONJ. R. (1963) Physiological responses to temperature in the lizard Crotaphytus collaris. Physiol. Zoiil. 36, 219-236. DAWSONW. R. & TEMPLETONJ. R. (1966) Physiological responses to temperature in the alligator lizard, Gerrhonotus multicarinatus. Ecology 47, 759-765. DEWITT C. B. (1967) Precision of thermoregulation and its relation to environmental factors in the desert iguana, Dipsosaurus dorsalis. Physiol. ZoiX 40,49-66. DICE L. R. & LERAASH. J. (1.936) A graphic method for comparing several sets of measurements. Contrib. Lab. Vert. Genetics U. Mich. No. 3, pp. l-3. GLAUERT L. (1961) A Handbook of the Lizards of Western Australia. West. Auat. Nat. Club Handbook, No. 6, Perth. HEATHJ. E. (1964) Head-body temperature differences in homed lizards. Physiol. Zoiil. 37, 273-279.

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HEATH J. E. (1965) Temperature regulation and diurnal activity in horned lizards. Univ. Calif. Publ. Zool. 64, 97-136. HEATWOLEH. (1970) Thermal ecology of the desert dragon Amphibolurus inermis. Ecol. Monogr. 40, 4254.57. HEATWOLEH., LIN T. H., VILLAL~N E., MUNIZ A. & MATTA A. (1969) Some aspects of the thermal ecology of Puerto Rican anoline lizards. J. Herpetology 3, 65-77. JACOBSONE. R. & WHITFORD W. G. (1971) Physiological responses to temperature in the patch-nosed snake, Salvadora hexalepis. Herpetologica 27, 289-295. JOHNSON C. R. (1972) Head-body temperature differences in Varanus gouldii (Sauria: Varanidae). Comp. Biochem. Physiol., 43A, 102.5-1029. LANGLOISJ. P. (1902) La regulation thermique chez les poikilothermes. r. Physiologie et de Pathologie generale 4, 249-256. LASHBROOKM. K. & LIVEZEY R. L. (1970) Effects of photoperiod on heat tolerance in Sceloporus occidentalis occidentalis. Physiol. ZoBI. 43, 38-46. LICHT P., DAWSONW. R., SHOEMAKERV. H. & MAIN A. R. (1966) Observations on the thermal relations of Western Australian Lizards. Copeia 1966, 97-l 10. MCGINNIS S. M. & BROWN C. W. (1966) Thermal behavior of the green iguana, Iguana iguana. Herpetologica 22, 184-l 89. MURRISH D. E. & VANCE V. J. (1968) Physiological responses to temperature acclimation in the lizard Uta mearnsi. Comp. Biochem. Physiol. 27, 329-337. RICHARDSS. A. (1970) The biology and comparative physiology of thermal panting. Biol. Rev. 45223-264. RUIBAL R. (1961) Thermal relations of five species of tropical lizards. Evol. 15, 98-l 11. SEXTON 0. J. & HEATWOLEH. (1968) An experimental investigation of habitat selection and water loss in some anoline lizards. Ecology 49,762-767. SPELLERBERGI. F. (1972) Temperature tolerances of southeast Australian reptiles examined in relation to reptile thermoregulatory behaviour and distribution. Oecologia 9, 23-46. STEBBINS R. C. (1961) Body temperature studies in South African lizards. Koedoe 4, 54-67. TEMPLETON J. R. (1960) Respiration and water loss at the higher temperatures in the desert iguana, Dipsosaurus dorsalis. Physiol. Zoiil. 33, 136-145. TEMPLETON J. R. & DAWSON W. R. (1963) Respiration in the lizard Crotaphytus collaris. Physiol. Zoiil. 36, 104-l 21. VERONJ. & HEATWOLEH. (1970) Temperature relations of the water skink, Sphenomorphus quoyi. J. Herpet. 4, 141-153. WARBURGM. R. (1965a) The influence of ambient temperature and humidity on the body temperature and water loss from two Australian lizards Tiliqua rugosa (Grey) (Scincidae) and Amphibolurus barbatus (Cuvier) (Agamidae). Aust.J. Zool. 13, 331-350. WARBURGM. R. (1965b) Studies on the environmental physiology of some Australian lizards from arid and semi-arid habitats. Aust._% ZooE. 13, 563475. WEBB G. J. W. & JOHNSON C. R. (1972) Head-body temperature differences in turtles. Comp. Biochem. Physiol., 43A, 593-611. WEBB G. J. W., JOHNSONC. R. & FIRTH B. T. (1972) Head-body temperature differences in lizards. Physiol. Zoiil. 45, 130-142. WILHOFT D. C. & ANDERSONJ. D. (1960) Effect of acclimation on the preferred body temperature of the lizard, Sceloporus occidentalis. Science, Wash. 131,610-611. WITTEN G. J. (1972) A new species of Amphibolurus from eastern Australia. Herpetologica 28,192-196. Key Word Index-Agamidae; Amphibolurus muricatus; &inks ; snakes ; temperature ; panting; panting threshold; reptilian thermoregulation; reptilian physiology; thermoregulation, head temperature.