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Heating and cooling rates in air and during diving of the Australian water skink, Sphenomorphus quoyii
Camp. Biochem. Physiol. Printed in Great Britain
Vol. UA,
No. 2, pp. 481492,
1987
0
0300-9629/87 1987 Pergamon
$3.00 + 0.00 Journals Ltd
HEATING AND COOLING RATES IN AIR AND DURING DIVING OF THE AUSTRALIAN WATER SKINK, SPHENOMORPHUS QUOYII CHRISTOPHER B. DANIELS,*
HAROLD
HEATWOLE
and
NICHOLAS
OAKES
Department of Zoology, University of New England, Armidale, N.S.W. 2351 Australia (Received 27 August 1986)
Abstract-l. Heating and cooling rates of a semiaquatic skink (Sphenomorphus quoyii) and a related terrestrial one (Crenotus robustus) were measured in air and during diving. 2. In air, all lizards cooled faster than they heated; all cooled faster in water than in air. 3. Dead water skinks in air heated as rapidly as they cooled; in water dead lizards cooled at similar rates to live ones during diving. 4. In air, adult S. quoyii had higher r values when heating and cooling than did Crenotus despite the greater surface area to volume ratio of the former. 5. Juvenile S. quoyii had smaller r values than either of the other two groups. 6. During diving, T values were similar for all these groups. 7. It would seem that physiological thermoregulation is ineffective in altering heat exchange in these small lizards when submerged. 8. In air, cooling occurs more rapidly than predicted from body size and may be influenced physiologically
INTRODUcTION
Almost all vital processes of reptiles are thermally dependent rate functions, and abrupt changes in body temperature would be expected to result in
marked alteration in capacity for normal biological activities. Indeed, many reptiles devote a considerable portion of their activity period in behaviorally regulating their body temperatures within rather precise, presumably optimal, limits [review by Heatwole and Taylor (1987)]. Accordingly, any species that is subjected to sudden, marked temperature fluctuations as a normal part of its daily life is of especial ecological and physiological interest. One such species is the Australian water skink, Sphenomorphus quoyii.
The water skink lives along the edges of streams and rivers in eastern Australia and inland via the Darling River system to northwestern Victoria and southeastern South Australia (Cogger, 1979). It is an escape diver, that is, when approached or molested by another animal it dives into the water and attempts to escape either by swimming away, or by diving to the bottom and remaining motionless there for a period of time (Daniels, 1984). In the environment in which it lives, this behavior often means that a lizard with a high body temperature leaves a site with warm substrate and air temperatures and plunges into much colder water. It would seem advantageous for such an animal to have mechanisms to reduce heat loss while submerged, thereby (1) maintaining its celerity and capacity for activity when re-emerging into what could still be a poten*Present address: Department of Physiology, School of Medicine, Flinders University of South Australia, Bedford Park S.A. 5042, Australia. Telephone (08)275-9911. 487 c B.P 87,ZA--R
tially dangerous situation and (2) reducing the time required to achieve its preferred temperature and concomitant optimal physiological function again. The purpose of the present paper is to compare and heating and cooling rates of this semi-aquatic species with those of a related, similarly-sized terrestrial skink (Ctenotus robustus) that does not use water or inhabit streamsides, but otherwise occurs in similar habitats in the same localities as the water skink. MATERIALS
AND METHODS
Lizards were collected by hand in January 1983 in the vicinity of Armidale, N.S.W., Australia, S. quoyii from the edges of creeks, and C. robusfus from adjacent terrestrial habitat. They were maintained in the laboratory in tanks containing materials appropriate to their natural habitat (for details see Daniels, 1984) until used in experiments the following May. For at least a week prior to experimentation, lizards were maintained at a photoperiod of 12L: 12D with daytime temperatures of 23-26°C and nocturnal ones of 1&15”C. They were fed on a variety of small invertebrates. Fifteen Ctenofus (87.3 & 1.97 mm SVL; 13.3 + 0.95 g). 15 adult S. quoyii (97.9 + 1.84 mm SVL; 18.4 _+0.98 g) and three juvenile S. quoyii (77.0 k 3.05 mm SVL; 8.3 k 1.03 g) were used. Each lizard used in experimentation was cold-anaesthetized by placing it in chipped ice. Then a copperconstantan thermocouple lead was inserted in the cloaca and connected to a digital display Comark electronic thermometer calibrated against a standard thermometer. The lizard was then placed in a clear perspex tube (27 cm long, 3.5 cm in diameter) which was then sealed with two rubber stoppers. The lead passed to the exterior through a hole in one of the stoppers which was made water tight with silicone gel. The thermocouple wire did not appear to unduly inconvenience the lizards. Heating and cooling proceeded in seven stages which were always undertaken in the same order:
488
CHRIST~P~R
1. The cold lizard was placed in the tube which was in turn put in a water bath at 36.6 f 0.32”C (termed the 30°C water bath) until the bodv temperature (T,) reached 30°C. Z.‘The lizard wab maintained at that body temperature for 5min. 3. The tube containing the lizard was removed from the 30°C water bath and placed in an adjacent water bath at 19.4 + 0.17”C (termed the 195°C water bath). One stopper was removed and the tube flooded with water. The lizard remained submerged for 12min, a time representing the mean voluntary diving time (6min) plus one standard deviation, at l%YC (daniels, 1984). 4. At the conclusion of the Itmin “dive” the lizard was removed from the 195°C bath, the tube drained of water
and the stopper replaced. The animal in its tube and breathing freely, was then placed in the 30°C bath until it had regained a body temperature of 30°C. 5. The lizard was maintained at a 30% body temperature for five min. 6. The lizard in the air-filled tube was tranferred to the 19S”C bath and cooled until its body temperature was identical to that reached at the conclusion of diving (usually between 20 and 205°C). 7. Finally, the air-filled tube containing the lizard was transferred to the 30°C water bath and reheated until the animal’s body temperature reached 30°C. Thus, the animals were heated in air, cooled submerged in water, re-heated in air, cooled in air, and heated in air once more; they were held at constant temperatures at intervals between each of these treatments. The bath temperatures of 30 and 19.5”C were chosen because they approximate mean air and water temperatures at creeks in the study region (Daniels, 1984). during the active season of lizards; furthermore, 30°C is similar to the preferred body temperature of both species (Heatwole,
3 DANIELS et al.
Fraser 1980). We chose to use r values, rather than temperature change per unit time because the change in core temperature in response to step function changes in ambient temperature is not linear but exponential, and therefore the rate of the temperature change is itself dependent on ambient temperature. Thus, data presented using rates of temperature change are only comparable between experiments of similar method. Use of the thermai time constant does not suffer from this disadvantage (Grian et al., 1979). Tau values were statistically analyzed king one-way analysis of variance and Student’s or Paired t-tests (Sokal and Rohlf, 1969). After experimentation, surface area to volume ratios were determined for 14 of the 15 S. q~~.vj~,and 12 of the 1.5 Ctenotus after killing them by freezing. Body volume was determined by immersing the lizards in a graduated cylinder filled with water. Orifices were sealed with adhesive prior to the volumetric determinations. The skin of each lizard was then removed and placed over graph paper graduated in mm. The body outline and that of the head, limbs, toes and tail were traced. Surface area was determined by counting the squares. RESULTS
There were no significant differences between the r values of the adult S. quuyii, juvenile S. quoyii and C. robustus during dives. However, adult S. guoyii exhibited significantly greater t values than did C. robustus or juvenile 3. quoyii in all other stages (Table 1). It seems somewhat surprising for S. quoyii to heat and cool more slowly than C. robustus because the former species possesses a significantly greater surface area to volume ratio (Fig. 1). Adults of S. quoyii cooled more rapidly during a 1976). Body temperature was recorded every I5 set during the dive than they did at rest in air, and they also cooled experiment. Thermal time constants, or tau (t) values, for faster than they heated. There were differences in the the heating and cooling rates of the lizards were determined rates of heating at rest and after the dive (Table 2). by semi-logarithmically plotting the differences between The dead S. quoyii exhibited t values not significantly ambient temperature (II’,) and body temperature (T,) over different from those obtained alive in all stages. The time. The thermal time constant can be defined as the time dead S. quoyii heated as rapidly as they cooled in min, for core temperature to change by 63% of the differential between Ts and r, at any particular time (tz) (t = 0.41, d.f. = 2, P > 0.05) but heated more slowly during the exponential approach of Ts to TA (Grigg, 1976: after a dive than at rest (t = 4.176, d.f. = 2, P < 0.0s) Smith, 1976, 1979; Crisp et al., 1979; Grigg et al., 1979; (Table 2). Juvenile S. quoyii also cooled faster underTable I. One-way analysis of variance of the Tau values of adult and juvenile Sphenomorphus quoyii and C~enofus robust during diving, heating after a dive and cooling and heating between 30 and 19.5 C Test Diving
Heating after a dive
Cooling
Heating
----
Group
5. quoyii adults S. quoyii juveniles C. roburtlrs
____~
Tau value Mean 1: SE 5.24 i: 0.090
W’f (15)
.._._~__
5.37 + 0.150
(3)
Error
Treatments
Analysis of variance df MS ss ~_~ ~_. ~-. .._.._ 0.52 2 0.26 28.00
30
5.02 j, 0.311
(15)
Total
28.52
32
1I .7s 2 0.741
(15)
Treatments
125.72
2
62.86
5.13 rto.130
(3)
Err01
199.11
30
6.64
9.24 + 0.632
(15)
Total
324.83
32
S. quoyii adults S. quoyii juveniles C. robusius
9.15 i:O.BS
(15)
Treatments
26.97
2
6.98 F 0.473
(3)
Error
55.01
30
13.49
P
~~0.05
9.47
10.05
7.35
8.48
to.05
1.83
7.43 t 0.418
(15)
Total
81.98
32
11.27 k 1.849
(15)
Treatments
109.35
2
54.67
5.44 rt 0.32
(3)
Error
193.45
30
6.45
8.56 k OS48
(15)
Total
302.80
32
Results presented as means + standard errors. Abbreviations are standard statistical notations.
F 0.28
0.93
S. puoyii adults S. quoyii juveniles C. robustus
S. quo@ adults s. quoyii juveniles C. robusrus
-
Heating and cooling of lizards
4J,
, 6
/ IO
,
,
,
12
,
r
,
14 16 VOLUME
,
,
I8 (ml)
,
,
,
,
20
22
24
Fig. 1. Relationship of surface area to volume in ;;yn+o;phus quoyii (A) and Ctenotus robust!! are: S. quoyu: equations regresslon robustus: r2 = 0.79. C. y = 4973.87 In x - 5123.02; y = 4530.24ln x -4413.93; r2 = 0.91.
water than in air but they heated faster than they cooled (Table 3). The juveniles did not exhibit significantly different values during heating at rest than during heating after a dive (Table 3). C. robustus
showed similar trends to those of adult S. quoyii. Ctenotus cooled faster in water than in air and they cooled faster than they heated (Table 3). No significant differences existed between the r values of Ctenotus heating after a dive and heating at rest (Table 3). Tau values increased with increased SVL and body mass for S. quoyii and C. robustus heating after a dive, and during heating and cooling at rest (Table 4). The relationships between body size and r value were not significant during diving. Thus C. robustus and juvenile S. quoyii heated and cooled faster than did adult water skinks. Generally, lizards (I) cooled faster than they heated, (2) heated after a dive at a similar rate to that at rest and (3) cooled faster in water than in air. The rate of heating and cooling in air, but not during diving, increased with increasing body size.
DISCUSSION
During diving, heat loss from the lizard was primarily by conduction. However, during heating in air the lizard received energy from the warm water by radiation and, to a lesser extent, by conduction. There probably were only small convectional air currents in the experimental chamber.
Table 2. Paired r-tests on the Tau values for adult Sphenomorphus conditions
Cooling underwater vs cooling Cooling vs heating Heating vs heating after a dive Diving Heating
after a dive
W)
r-value
df
P
5.24 k 0.190 9.15kO.285 9.15+0.285 I 1.27f 1.849 I I .27 + I .849 II.75 + 0.741
(15) (15) (15) (15) (15) (15)
13.81
14
<0.05
2.46
I4
<0.05
0.83
I4
>0.0.5
Alive Dead
5.68 k 0.177 4.80 + 1.084
(3) (3)
0.78
2
z 0.05
Alive
8.29f 0.830
(3)
0.29
2
>0.05
2.74
2
>0.05
0.86
2
> 0.05
Diving Cooling Cooling Heating Heating *Heating wet
8.53 f 10.40 f 7.81 k 9.00 i 7.46+
Dead Alive Dead Alive Dead
Cooling Heating
quoyii under different experimental
Tau value Mean f SE
Group
Test
489
0.237 0.429 0.730 0.789 I.016
(3) (3) (3) (3) (3)
The top half of the table is the analysis of live S. quoyii heating or cooling during the different experimental procedures. In the bottom portion, heating and cooling rates of live S. quoyii are compared against the equivalent rates after death. *Heating of wet animal.
Table 3. Paired I-tests on the Tau values for juvenile Sphenomorphus under different experimental conditions Test
Tau value Mean + SE
Group Juvenile
Cooling underwater vs cooling Cooling vs heating Heating vs heating after a dive Cooling underwater vs cooling Cooling vs heating Heating vs heating after a dive ‘Heating
of wet animal.
Diving Cooling Cooling Heating Heating *Heating
wet
Diving Cooling Coolinn Heatin;; Heating *Heating wet
Sphenomorphus 5.37 k 0.150 6.98 i 0.473 6.98 * 0.473 5.44 f 0.320 5.44 f 0.320 5.13*0.130 Ctenotus 5.02 * 7.43 + 7.43 + 8.56: 8.56 f 9.24 k
robustus 0.3 I I 0.418 0.418 0.548 0.548 0.632
W) quoyii (3) (3) (3) (3) (3) (3) (15) (15) (15) ilsj (15) (15)
quoyii and Ctenoms robustus
I -value
df
P
4.33
2
co.05
4.84
2
<0.05
I .63
2
>0.05
4.68
I4
<0.05
2.27
I4
<0.05
I .20
I4
>0.05
490
CHRISTOPHER
B.
DANIELSet
al.
Table 4. Regressions of snout-vent length and body mass against Tao values for Sphenomorphus quoyii and Crenorus robustus
Experimental conditions
Sphenomorphus
Regression
quoyii
N
r2
Diving Heating after a dive Cooling Heating
Snout-vent length regressed against y =0.02x + 3.52 18 0.08 .v = 0.18~ -6.55 I8 0.27* I8 .v = 0.08x + I .08 0.41* y =0.17x -6.21 18 0.26*
Diving Heating after a dive Cooling Heating
I’ = 0.02x )’ = 0.53x ,v =0.16x Y =0.32x
*Indicates
significant
CltVllJtUS robustus N
Regression r-value 1’= 0.05x :v = 0.18x .v =0.14.x )’ = 0.21x
12
+ 0.55 ~ 6.24 -4.39 - 9.38
15 I5 15 I5
0.1 I 0.311 0.41* 0.55’
Bodv mass rezressed azainst r-value + 4.96 ’ 180.02 I‘ =0.10x + 3.74 + I .79 18 0.57* 1’ = 0.39x + 4.06 +6.15 I8 0.38’ 4’ =0.35x + 2.75 + 5.57 18 0.18 I’ = 0.39x + 3.31
I5 I5 15 I5
0.09 0.34’ 0.64’ 0.47’
value (P < 0.05).
Grigg and Alchin (1976) suggested that because of the high specific heat of water, aquatic reptiles have greater difficulty than terrestrial species in retarding heat loss and might exhibit superior mechanisms for heat retention. However, despite significant differences in cooling rates in air, adult and juvenile water skinks and Ctenotus exhibit similar r values (approximately 5 min) when cooling underwater. Such high values differ greatly from those predicted by regressing T values against body mass for lizards in water but not diving (Grigg et al., 1979; Smith et al., 1984). Using Grigg et d’s (1979) regression for “lizard shaped reptiles” cooling in water (i.e. In t = - 2.07 + 0.66 1nM) then lizards with a mass of 18 g have a r value of 0.69min while 13 and 8-g lizards have predicted 7 values of 0.42 and 0.20 min, respectively. Smith et ~1,‘s (1984) regression for alligators cooling in water (r = 12.61 i@62) predicts that if such tiny alligators could be found, an 18-g one would have a 7 value of 1.06 min, a 13-g alligator would possess a 7 of 0.87 min and the r value of a 9-g alligator would be 0.69min. Intuitively these predicted values appear to be feasible because the high surface area to volume ratios of very small reptiles would be expected to promote rapid heat exchange in cold water. However, the three groups examined in this study gave much larger r values than those predicted for animals of their mass cooling in water but not diving. The regressions of Grigg et al. (1979) and Smith et al. (1984) may be poor predictors of the 7 values of very small lizards because they are based on larger or specialized reptiles and their animals were not diving. Grigg et al. (1979) based their regression on data from reptiles greater than 1OOg. The smallest of Smith et al’s (1984) alligators was 37 g and alligators may also possess a greater capacity for physiological thermoregulation in water than equivalent-sized lizards (Grigg and Alchin, 1976; Smith, 1979). Interestingly, Tiliqun scincoides (mean mass 413.7 g) and Physignathus lesueurii (mean mass 305.5 g) exhibited mean 7 values for cooling in water of 7.56 min and 5.76min respectively (Grigg et al., 1979; Fraser, 1980), which are very similar to the diving values of S. quoyii and C. robustus. Moreover, the rates of cooling while diving for living and dead S. quoyii were not significantly different. While our study and that of Fraser and Grigg (1984) indicate large mass-related intraspecific variability in lizard 7 values, it may be that the z values for all lizards below approximately 500 g cooling in water are ap-
proximately 5 min. It seems unlikely therefore that physiological thermoregulation affects the rate of cooling for small lizards in water whether diving or breathing. Both S. quoyii and Ctenotus heat at the same rate after a dive as when heating without prior diving. This result is surprising as the lizards differ in several potentially influential ways under these two treatments. First, after diving the lizards were wet and some of the initial heat should have been dissipated through evaporation of water from the body surface. Second, S. quoyii and Ctenotus have elevated ventilatory rates after diving (Daniels et al., 1987). Such increased rates of ventilation have frequently been associated with reduced heating rates because of concomitant evaporative cooling from respiratory surfaces (Barthlolmew and Tucker, 1963; Bartholomew et al., 1965; Grigg and Alchin, 1976; Wood and Lenfant, 1976; Bartholomew, 1982). In the present study, not only were there no significant differences in heating rates between lizards that had previously dived and those that had not, but dead lizards after a “dive” heated as rapidly as living ones. Clearly, evaporative cooling either of the skin or the respiratory surfaces was negligible in its effect on heating rates under the experimental conditions of this study. Physiological thermoregulation of reptiles in air has been reviewed by Grigg and Alchin (1976) Jammes and Grimaud (1976), Smith (1976, 1979); Crawshaw (1979), Huey and Stevenson (1979), Bartholomew and Vleck (1979), Bartholomew (1982) and Heatwole and Taylor (1987). In general, reptiles heat more rapidly than they cool, particularly in humid air, and they exhibit higher heart rates, rates of oxygen consumption and ventilation frequencies during heating than during cooling. The increased heart rate is associated with greater peripheral blood flow enabling a more rapid heat transfer from the exterior to the body core. Metabolic heat production usually contributes a small but variable influence on the rate of heating, and is more important in larger reptiles. Larger animals possess a greater capacity for physiological thermoregulation than do smaller ones. However, exceptions exist for each of these generalizations. Some reptiles, especially very small ones, cool faster than they heat (Spray and May, 1972; Grigg ef al., 1979; Fraser and Grigg, 1984; Fraser, 1980), do not always change heart rate with body temperature (Jacob and McDonald, 1975), or do not alter ventilation frequency with change in body tem-
Heating and cooling of lizards
491
Table 5. The relationship between Tan values and body weight for small lizards (< 20 g) heating and cooling in air
Tau heating (min)
Tan cooling (min) Mean i_ SE
Mass (g) Mean + SE
N
Mean + SE
0.939 * 0.054
IO
4.129 f 0.302
L. guichenoti
I.189 kO.076
I5
3.744 * 0.194
3.206+0.119
L. mustelina
2.501 * 0.159
7
4.694 f
0.330
4. I80 + 0.349
4.979 & 0.274 8.33 k I .03 12.755 + I.155 13.31 * 0.95 18.37 i 0.98
IO 3 2 I5 I5
6. I89 + 5.44 k I I .OOi 8.56 + ll.27*
0.384 0.320 0.750 0.548 1.849
5.485 + 0.300 6.98 f 0.473 10.85 + 0.349 7.43 i 0.418 9.l5fO.285
Species Lampropholis
Ctenotus
delicata
taeniolatus
Sphenomorphus
S.
quoyii
(juveniles)
quoyii
(adults)
tympanum
Ctenotus
robustus
Sphenomorphus
3.238 + 0.196
Reference Fraser (1980) Fraser (I 980) Fraser ( 1980) Fraser (I 980) This Study Fraser (1980) This Study This Study
The regression equations are: Source This Study Gregg et al. (1979) Smith (1976) Gregg et al. (1979) Smith ct al. (1984)
Animals <2og “lizard shaped reptiles” > 100 g Alligators 6C-764 g “lizard shaped reptiles” > 100 g Alligators 37-103 kg
M = mass, in grams, in all studies except Smith
Medium
N
air air air water water
8 9 I3 9 22
Heating In 7 = I .29 + 0.35 In M In z = 0.72 + 0.36 In M In r = 0.415 + 0.328 In M In r = 2. I I + 0.61 In M r = 8.81 MO50
Cooling Inr=l.l3+0.39InM In r = 0.42 + 0.44 In M In r = 0.237 + 0.433 In M Inr = -2.07f0.66InM r = 12.61 Mo6’
et al. (1984) where M is in kg.
perature (Bennett, 1973; Snyder and Weathers, 1976). Moreover, some species exhibit elevated heart rates during heating which do not influence the rate of temperature change (Weathers and White 1971; Lucey 1974). S. quoyii and Ctenotus both exhibit physiological thermoregulatory responses that differ from the general pattern in two ways: (1) their heart rate and ventilatory responses are ineffective in controlling heating and cooling rates and (2) they cool faster than they heat. These will be discussed in turn. S. quoyii and C. robustus exhibited higher heart rates and breathing rates during heating than during cooling (Daniels et al., 1987) but cooled faster than they heated. Moreover, dead lizards heated and cooled at the same rate as living ones. Such a response negates the hypothesis that increases in heart and breathing rates affect the thermoregulatory process. Heart rate may increase during heating, thereby maintaining blood pressure which otherwise would decrease in response to peripheral vasodilation (White, 1976). Cooling may stimulate cutaneous vasoconstriction which also may reflexly affect blood pressure. The function of the differences in ventilation rates is unknown, but may reflect differences in oxygen consumption. Bartholomew and Vleck (1979) observed Amblyrhynchus cristatus to consume more oxygen during heating than during cooling, but this remains to be verified for smaller lizards. Both S. quoyii and C. robustus cooled faster than they heated. The trends in heating and cooling may be related to body size. If the 5 values for heating and cooling are regressed against body size for lizardshaped reptiles larger than 100 g (Grigg et al., 1979) or alligators larger than 60 g (Smith, 1976) (Table 4), as body mass decreases, both reveal relatively smaller 7 values during heating than during cooling. The regressions intersect (7 heating = 7 cooling) at a body weight of 46 g using the equations of Grigg et al. (1979) and at one of 42 g using that of Smith (1976). Using our data on S. quoyii and C. robustus and the 5 values for several other small skinks (Fraser, 1980; Fraser and Grigg, 1984) the regression lines intersect at 48 g (Table 5). These results consistently predict that lizards smaller than 40-5Og should cool faster than they heat. It has often been argued that the
ability to heat faster than cool is advantageous and under physiological control, but that the converse represents the absence of any physiological capacity to control body temperature (Bartholomew, 1982). However, very small, dead lizards heat and cool at the same rate (Fraser, 1980; Table 5). Hence the ability to cool faster than heat, may be under some physiological control. The nature of such physiological processes still remains to be determined. Acknowledgements-We are grateful to the Commonwealth Postgraduate Scholarship Fund for financial support (to
C.B.D.). Sandra Higgins typed the manuscript, Lynda Bridges prepared the figure and Maria McCoy and Russell Hobbs provided technical assistance and help with the computing. REFERENCES
Bartholomew G. A. (1982) Physiological control of body temperature. In Biology of rhe Reptilia (Edited by Gans C. and Pugh F. H.), Vol. 12, pp. 167-212. Academic Press, London. Bartholomew G. A. and Tucker V. A. (1963) Control of changes in body temperature, metabolism and circulation by the agamid lizard Amphibolurus barbatus. Physiol. Zool. 36, 199-218. Bartholomew G. A., Tucker V. A. and Lee A. K. (1965) Oxygen consumption, thermal conductance and heart rate in the Australian Skink Tiliqua scincoides. Copeia 1%5, 169-173.
Bartholomew, G. A. and Vleck D. (1979) The relation of oxygen consumption to body size and to heating and cooling in the Galapagos marine iguana Amblyrhynchus crisfatus. J. camp. Physiol. 132, 285-288.
Bennett A. F. (1973) Ventilation in two species of lizards during rest and activity. Camp. Biochem. Physiol. 46A, 653-67 1. Cogger H. G. (1979) Reptiles and Amphibians of Australia, 2nd edn. Reed, Sydney. Crawshaw L. I. (1979) Responses to rapid temperature change in vertebrate ectotherms. Am. Zool. 19, 225-237. Crisp M., Cook L. M. and Hereward F. V. (1979) Colour
and heat balance in the lizard Lucerta dugesii. Copeia 1979, 250-257.
Daniels C. B. (1984) The adaptations to a riparian habitat by the water skink Sphenomorphus quoyii. Ph.D. Thesis, University of New England. Daniels C. B., Oakes N. and Heatwole H. (1987) Physiological diving adaptations of the Australian water
492
CHRISTOPHERB.
skink, Sphenomorphus auovii. Comp. Biochem. Physiol. A (in press).
Fraser S. P. (1980) Insights into the physiological and behavioural thermoregulatory abilities of small lizards. B.Sc.(Hons) Thesis, University of Sydney. Fraser S. P. and Grirrg G. C. (1984) Control of thermal conductance is ins@ficant td ther~oregulation in small reptiles. P~~~io~~Zool. 57, 392400. Grigg G. C. (1976) Practical notes and comments on the application of X, the thermal time constant, to analysis of responses by reptiles to step function increases or decreases in ambient temperature. University of Queensland, Department of Zoology Practical Notes, Brisbane, Queensland. Grigg G. C. and Alchin J. (1976) The role of the cardiovascular system in the thermoregulation of Crocodylus johnstoni. Zoology 49, 24-36. Grigg G. C., Drane R. and Courtice G. P. (1979) Time constants of heating and cooling in the eastern water dragon Physignathus Iesueurii and some generalizations about heating and cooling in reptiles, J. Therm. Biol. 4, 95-103.
Heatwoie H. (1976) Repfjle Ecology. University of Queensland Press, St. Lucia. Heatwole H. and Taylor J. (1987) Ecology of Reptiles. University of Queensland Press, St. Lucia. (In press). Huey R. 8. and Stevenson R. D. (1979) Integrating thermal p~ysioIogy and ecology of ectotherms. A discussion of armroaches. Am. Zool. 19, 357-366. Jacob J. S. and McDonald H. S. (1975) Diving bradycardia in four species of North American aquatic snakes. Comp. Biochem. Physiol. 53A, 69-72.
DANIELSet al. Jammes Y. and Grimaud C. (1976) Ventilation, pulmonary and cutaneous gas exchange in the awake lizards Lucerra airi& Camp. Biochem. Physiol. !%A, 279-285. Lucey E. C. (1974) Heart rates and physiological thermoregulation in a basking turtle Psuedemys scripta elegans. Comp. Biochem. Physiol. 48A, 471482. Smith E. N. (1976) Heating and cooling rates of the American alligator, AIIigutor m~s~ss~ppiensis, Physiol. ZOOI. 49, 37-48.
Smith E. N. (1979) Behavioural and physiological thermoregulation of crocodilians. Am. 2001. 19, 239-247. Smith E. N., Standora E. A. and Robertson S. L. (1984) Physiological thermoregulation of mature alligators. Comu. Biochem. Phvsiol. 77A, 189--193.
Snyder. G. K. and Weathers W. W. (1976) Physiological responses to temperature in the tropical lizard Hemidactylus~enatus (Sauria: Gekkonidae). Herpetologica 32, 252-256. Sokal R. R. and Rohlf F. J. (1969) Introduction to Biosfatistics. W. H. Freeman and Co., San Francisco. Spray D. C. and May M. L. (1972) Heating and cooling rates in four species of turtles. Comp. Biochem. PItysiol. 41 A, 507-522.
Weathers W. W. and White F. N. (1971) Physiological thermoregulation in turtles. Am. I. Physiol. 221,704710. White F. N. (1976) Circulation. In Biology of the Reptilia (Edited by Gans C. and Dawson W. R.), Vol. 5, pp. 275-334. Academic Press. London. Wood S. C. and Lenfant C. J. M. (1976) Respiration: Mechanics, control and gas exchange. In BioIogy of the Reptilia (Edited by Gans C. and Dawson W. R.), Vol. 5, pp. 225-274. Academic Press, London.
Vol. UA,
No. 2, pp. 481492,
1987
0
0300-9629/87 1987 Pergamon
$3.00 + 0.00 Journals Ltd
HEATING AND COOLING RATES IN AIR AND DURING DIVING OF THE AUSTRALIAN WATER SKINK, SPHENOMORPHUS QUOYII CHRISTOPHER B. DANIELS,*
HAROLD
HEATWOLE
and
NICHOLAS
OAKES
Department of Zoology, University of New England, Armidale, N.S.W. 2351 Australia (Received 27 August 1986)
Abstract-l. Heating and cooling rates of a semiaquatic skink (Sphenomorphus quoyii) and a related terrestrial one (Crenotus robustus) were measured in air and during diving. 2. In air, all lizards cooled faster than they heated; all cooled faster in water than in air. 3. Dead water skinks in air heated as rapidly as they cooled; in water dead lizards cooled at similar rates to live ones during diving. 4. In air, adult S. quoyii had higher r values when heating and cooling than did Crenotus despite the greater surface area to volume ratio of the former. 5. Juvenile S. quoyii had smaller r values than either of the other two groups. 6. During diving, T values were similar for all these groups. 7. It would seem that physiological thermoregulation is ineffective in altering heat exchange in these small lizards when submerged. 8. In air, cooling occurs more rapidly than predicted from body size and may be influenced physiologically
INTRODUcTION
Almost all vital processes of reptiles are thermally dependent rate functions, and abrupt changes in body temperature would be expected to result in
marked alteration in capacity for normal biological activities. Indeed, many reptiles devote a considerable portion of their activity period in behaviorally regulating their body temperatures within rather precise, presumably optimal, limits [review by Heatwole and Taylor (1987)]. Accordingly, any species that is subjected to sudden, marked temperature fluctuations as a normal part of its daily life is of especial ecological and physiological interest. One such species is the Australian water skink, Sphenomorphus quoyii.
The water skink lives along the edges of streams and rivers in eastern Australia and inland via the Darling River system to northwestern Victoria and southeastern South Australia (Cogger, 1979). It is an escape diver, that is, when approached or molested by another animal it dives into the water and attempts to escape either by swimming away, or by diving to the bottom and remaining motionless there for a period of time (Daniels, 1984). In the environment in which it lives, this behavior often means that a lizard with a high body temperature leaves a site with warm substrate and air temperatures and plunges into much colder water. It would seem advantageous for such an animal to have mechanisms to reduce heat loss while submerged, thereby (1) maintaining its celerity and capacity for activity when re-emerging into what could still be a poten*Present address: Department of Physiology, School of Medicine, Flinders University of South Australia, Bedford Park S.A. 5042, Australia. Telephone (08)275-9911. 487 c B.P 87,ZA--R
tially dangerous situation and (2) reducing the time required to achieve its preferred temperature and concomitant optimal physiological function again. The purpose of the present paper is to compare and heating and cooling rates of this semi-aquatic species with those of a related, similarly-sized terrestrial skink (Ctenotus robustus) that does not use water or inhabit streamsides, but otherwise occurs in similar habitats in the same localities as the water skink. MATERIALS
AND METHODS
Lizards were collected by hand in January 1983 in the vicinity of Armidale, N.S.W., Australia, S. quoyii from the edges of creeks, and C. robusfus from adjacent terrestrial habitat. They were maintained in the laboratory in tanks containing materials appropriate to their natural habitat (for details see Daniels, 1984) until used in experiments the following May. For at least a week prior to experimentation, lizards were maintained at a photoperiod of 12L: 12D with daytime temperatures of 23-26°C and nocturnal ones of 1&15”C. They were fed on a variety of small invertebrates. Fifteen Ctenofus (87.3 & 1.97 mm SVL; 13.3 + 0.95 g). 15 adult S. quoyii (97.9 + 1.84 mm SVL; 18.4 _+0.98 g) and three juvenile S. quoyii (77.0 k 3.05 mm SVL; 8.3 k 1.03 g) were used. Each lizard used in experimentation was cold-anaesthetized by placing it in chipped ice. Then a copperconstantan thermocouple lead was inserted in the cloaca and connected to a digital display Comark electronic thermometer calibrated against a standard thermometer. The lizard was then placed in a clear perspex tube (27 cm long, 3.5 cm in diameter) which was then sealed with two rubber stoppers. The lead passed to the exterior through a hole in one of the stoppers which was made water tight with silicone gel. The thermocouple wire did not appear to unduly inconvenience the lizards. Heating and cooling proceeded in seven stages which were always undertaken in the same order:
488
CHRIST~P~R
1. The cold lizard was placed in the tube which was in turn put in a water bath at 36.6 f 0.32”C (termed the 30°C water bath) until the bodv temperature (T,) reached 30°C. Z.‘The lizard wab maintained at that body temperature for 5min. 3. The tube containing the lizard was removed from the 30°C water bath and placed in an adjacent water bath at 19.4 + 0.17”C (termed the 195°C water bath). One stopper was removed and the tube flooded with water. The lizard remained submerged for 12min, a time representing the mean voluntary diving time (6min) plus one standard deviation, at l%YC (daniels, 1984). 4. At the conclusion of the Itmin “dive” the lizard was removed from the 195°C bath, the tube drained of water
and the stopper replaced. The animal in its tube and breathing freely, was then placed in the 30°C bath until it had regained a body temperature of 30°C. 5. The lizard was maintained at a 30% body temperature for five min. 6. The lizard in the air-filled tube was tranferred to the 19S”C bath and cooled until its body temperature was identical to that reached at the conclusion of diving (usually between 20 and 205°C). 7. Finally, the air-filled tube containing the lizard was transferred to the 30°C water bath and reheated until the animal’s body temperature reached 30°C. Thus, the animals were heated in air, cooled submerged in water, re-heated in air, cooled in air, and heated in air once more; they were held at constant temperatures at intervals between each of these treatments. The bath temperatures of 30 and 19.5”C were chosen because they approximate mean air and water temperatures at creeks in the study region (Daniels, 1984). during the active season of lizards; furthermore, 30°C is similar to the preferred body temperature of both species (Heatwole,
3 DANIELS et al.
Fraser 1980). We chose to use r values, rather than temperature change per unit time because the change in core temperature in response to step function changes in ambient temperature is not linear but exponential, and therefore the rate of the temperature change is itself dependent on ambient temperature. Thus, data presented using rates of temperature change are only comparable between experiments of similar method. Use of the thermai time constant does not suffer from this disadvantage (Grian et al., 1979). Tau values were statistically analyzed king one-way analysis of variance and Student’s or Paired t-tests (Sokal and Rohlf, 1969). After experimentation, surface area to volume ratios were determined for 14 of the 15 S. q~~.vj~,and 12 of the 1.5 Ctenotus after killing them by freezing. Body volume was determined by immersing the lizards in a graduated cylinder filled with water. Orifices were sealed with adhesive prior to the volumetric determinations. The skin of each lizard was then removed and placed over graph paper graduated in mm. The body outline and that of the head, limbs, toes and tail were traced. Surface area was determined by counting the squares. RESULTS
There were no significant differences between the r values of the adult S. quuyii, juvenile S. quoyii and C. robustus during dives. However, adult S. guoyii exhibited significantly greater t values than did C. robustus or juvenile 3. quoyii in all other stages (Table 1). It seems somewhat surprising for S. quoyii to heat and cool more slowly than C. robustus because the former species possesses a significantly greater surface area to volume ratio (Fig. 1). Adults of S. quoyii cooled more rapidly during a 1976). Body temperature was recorded every I5 set during the dive than they did at rest in air, and they also cooled experiment. Thermal time constants, or tau (t) values, for faster than they heated. There were differences in the the heating and cooling rates of the lizards were determined rates of heating at rest and after the dive (Table 2). by semi-logarithmically plotting the differences between The dead S. quoyii exhibited t values not significantly ambient temperature (II’,) and body temperature (T,) over different from those obtained alive in all stages. The time. The thermal time constant can be defined as the time dead S. quoyii heated as rapidly as they cooled in min, for core temperature to change by 63% of the differential between Ts and r, at any particular time (tz) (t = 0.41, d.f. = 2, P > 0.05) but heated more slowly during the exponential approach of Ts to TA (Grigg, 1976: after a dive than at rest (t = 4.176, d.f. = 2, P < 0.0s) Smith, 1976, 1979; Crisp et al., 1979; Grigg et al., 1979; (Table 2). Juvenile S. quoyii also cooled faster underTable I. One-way analysis of variance of the Tau values of adult and juvenile Sphenomorphus quoyii and C~enofus robust during diving, heating after a dive and cooling and heating between 30 and 19.5 C Test Diving
Heating after a dive
Cooling
Heating
----
Group
5. quoyii adults S. quoyii juveniles C. roburtlrs
____~
Tau value Mean 1: SE 5.24 i: 0.090
W’f (15)
.._._~__
5.37 + 0.150
(3)
Error
Treatments
Analysis of variance df MS ss ~_~ ~_. ~-. .._.._ 0.52 2 0.26 28.00
30
5.02 j, 0.311
(15)
Total
28.52
32
1I .7s 2 0.741
(15)
Treatments
125.72
2
62.86
5.13 rto.130
(3)
Err01
199.11
30
6.64
9.24 + 0.632
(15)
Total
324.83
32
S. quoyii adults S. quoyii juveniles C. robusius
9.15 i:O.BS
(15)
Treatments
26.97
2
6.98 F 0.473
(3)
Error
55.01
30
13.49
P
~~0.05
9.47
10.05
7.35
8.48
to.05
1.83
7.43 t 0.418
(15)
Total
81.98
32
11.27 k 1.849
(15)
Treatments
109.35
2
54.67
5.44 rt 0.32
(3)
Error
193.45
30
6.45
8.56 k OS48
(15)
Total
302.80
32
Results presented as means + standard errors. Abbreviations are standard statistical notations.
F 0.28
0.93
S. puoyii adults S. quoyii juveniles C. robustus
S. quo@ adults s. quoyii juveniles C. robusrus
-
Heating and cooling of lizards
4J,
, 6
/ IO
,
,
,
12
,
r
,
14 16 VOLUME
,
,
I8 (ml)
,
,
,
,
20
22
24
Fig. 1. Relationship of surface area to volume in ;;yn+o;phus quoyii (A) and Ctenotus robust!! are: S. quoyu: equations regresslon robustus: r2 = 0.79. C. y = 4973.87 In x - 5123.02; y = 4530.24ln x -4413.93; r2 = 0.91.
water than in air but they heated faster than they cooled (Table 3). The juveniles did not exhibit significantly different values during heating at rest than during heating after a dive (Table 3). C. robustus
showed similar trends to those of adult S. quoyii. Ctenotus cooled faster in water than in air and they cooled faster than they heated (Table 3). No significant differences existed between the r values of Ctenotus heating after a dive and heating at rest (Table 3). Tau values increased with increased SVL and body mass for S. quoyii and C. robustus heating after a dive, and during heating and cooling at rest (Table 4). The relationships between body size and r value were not significant during diving. Thus C. robustus and juvenile S. quoyii heated and cooled faster than did adult water skinks. Generally, lizards (I) cooled faster than they heated, (2) heated after a dive at a similar rate to that at rest and (3) cooled faster in water than in air. The rate of heating and cooling in air, but not during diving, increased with increasing body size.
DISCUSSION
During diving, heat loss from the lizard was primarily by conduction. However, during heating in air the lizard received energy from the warm water by radiation and, to a lesser extent, by conduction. There probably were only small convectional air currents in the experimental chamber.
Table 2. Paired r-tests on the Tau values for adult Sphenomorphus conditions
Cooling underwater vs cooling Cooling vs heating Heating vs heating after a dive Diving Heating
after a dive
W)
r-value
df
P
5.24 k 0.190 9.15kO.285 9.15+0.285 I 1.27f 1.849 I I .27 + I .849 II.75 + 0.741
(15) (15) (15) (15) (15) (15)
13.81
14
<0.05
2.46
I4
<0.05
0.83
I4
>0.0.5
Alive Dead
5.68 k 0.177 4.80 + 1.084
(3) (3)
0.78
2
z 0.05
Alive
8.29f 0.830
(3)
0.29
2
>0.05
2.74
2
>0.05
0.86
2
> 0.05
Diving Cooling Cooling Heating Heating *Heating wet
8.53 f 10.40 f 7.81 k 9.00 i 7.46+
Dead Alive Dead Alive Dead
Cooling Heating
quoyii under different experimental
Tau value Mean f SE
Group
Test
489
0.237 0.429 0.730 0.789 I.016
(3) (3) (3) (3) (3)
The top half of the table is the analysis of live S. quoyii heating or cooling during the different experimental procedures. In the bottom portion, heating and cooling rates of live S. quoyii are compared against the equivalent rates after death. *Heating of wet animal.
Table 3. Paired I-tests on the Tau values for juvenile Sphenomorphus under different experimental conditions Test
Tau value Mean + SE
Group Juvenile
Cooling underwater vs cooling Cooling vs heating Heating vs heating after a dive Cooling underwater vs cooling Cooling vs heating Heating vs heating after a dive ‘Heating
of wet animal.
Diving Cooling Cooling Heating Heating *Heating
wet
Diving Cooling Coolinn Heatin;; Heating *Heating wet
Sphenomorphus 5.37 k 0.150 6.98 i 0.473 6.98 * 0.473 5.44 f 0.320 5.44 f 0.320 5.13*0.130 Ctenotus 5.02 * 7.43 + 7.43 + 8.56: 8.56 f 9.24 k
robustus 0.3 I I 0.418 0.418 0.548 0.548 0.632
W) quoyii (3) (3) (3) (3) (3) (3) (15) (15) (15) ilsj (15) (15)
quoyii and Ctenoms robustus
I -value
df
P
4.33
2
co.05
4.84
2
<0.05
I .63
2
>0.05
4.68
I4
<0.05
2.27
I4
<0.05
I .20
I4
>0.05
490
CHRISTOPHER
B.
DANIELSet
al.
Table 4. Regressions of snout-vent length and body mass against Tao values for Sphenomorphus quoyii and Crenorus robustus
Experimental conditions
Sphenomorphus
Regression
quoyii
N
r2
Diving Heating after a dive Cooling Heating
Snout-vent length regressed against y =0.02x + 3.52 18 0.08 .v = 0.18~ -6.55 I8 0.27* I8 .v = 0.08x + I .08 0.41* y =0.17x -6.21 18 0.26*
Diving Heating after a dive Cooling Heating
I’ = 0.02x )’ = 0.53x ,v =0.16x Y =0.32x
*Indicates
significant
CltVllJtUS robustus N
Regression r-value 1’= 0.05x :v = 0.18x .v =0.14.x )’ = 0.21x
12
+ 0.55 ~ 6.24 -4.39 - 9.38
15 I5 15 I5
0.1 I 0.311 0.41* 0.55’
Bodv mass rezressed azainst r-value + 4.96 ’ 180.02 I‘ =0.10x + 3.74 + I .79 18 0.57* 1’ = 0.39x + 4.06 +6.15 I8 0.38’ 4’ =0.35x + 2.75 + 5.57 18 0.18 I’ = 0.39x + 3.31
I5 I5 15 I5
0.09 0.34’ 0.64’ 0.47’
value (P < 0.05).
Grigg and Alchin (1976) suggested that because of the high specific heat of water, aquatic reptiles have greater difficulty than terrestrial species in retarding heat loss and might exhibit superior mechanisms for heat retention. However, despite significant differences in cooling rates in air, adult and juvenile water skinks and Ctenotus exhibit similar r values (approximately 5 min) when cooling underwater. Such high values differ greatly from those predicted by regressing T values against body mass for lizards in water but not diving (Grigg et al., 1979; Smith et al., 1984). Using Grigg et d’s (1979) regression for “lizard shaped reptiles” cooling in water (i.e. In t = - 2.07 + 0.66 1nM) then lizards with a mass of 18 g have a r value of 0.69min while 13 and 8-g lizards have predicted 7 values of 0.42 and 0.20 min, respectively. Smith et ~1,‘s (1984) regression for alligators cooling in water (r = 12.61 i@62) predicts that if such tiny alligators could be found, an 18-g one would have a 7 value of 1.06 min, a 13-g alligator would possess a 7 of 0.87 min and the r value of a 9-g alligator would be 0.69min. Intuitively these predicted values appear to be feasible because the high surface area to volume ratios of very small reptiles would be expected to promote rapid heat exchange in cold water. However, the three groups examined in this study gave much larger r values than those predicted for animals of their mass cooling in water but not diving. The regressions of Grigg et al. (1979) and Smith et al. (1984) may be poor predictors of the 7 values of very small lizards because they are based on larger or specialized reptiles and their animals were not diving. Grigg et al. (1979) based their regression on data from reptiles greater than 1OOg. The smallest of Smith et al’s (1984) alligators was 37 g and alligators may also possess a greater capacity for physiological thermoregulation in water than equivalent-sized lizards (Grigg and Alchin, 1976; Smith, 1979). Interestingly, Tiliqun scincoides (mean mass 413.7 g) and Physignathus lesueurii (mean mass 305.5 g) exhibited mean 7 values for cooling in water of 7.56 min and 5.76min respectively (Grigg et al., 1979; Fraser, 1980), which are very similar to the diving values of S. quoyii and C. robustus. Moreover, the rates of cooling while diving for living and dead S. quoyii were not significantly different. While our study and that of Fraser and Grigg (1984) indicate large mass-related intraspecific variability in lizard 7 values, it may be that the z values for all lizards below approximately 500 g cooling in water are ap-
proximately 5 min. It seems unlikely therefore that physiological thermoregulation affects the rate of cooling for small lizards in water whether diving or breathing. Both S. quoyii and Ctenotus heat at the same rate after a dive as when heating without prior diving. This result is surprising as the lizards differ in several potentially influential ways under these two treatments. First, after diving the lizards were wet and some of the initial heat should have been dissipated through evaporation of water from the body surface. Second, S. quoyii and Ctenotus have elevated ventilatory rates after diving (Daniels et al., 1987). Such increased rates of ventilation have frequently been associated with reduced heating rates because of concomitant evaporative cooling from respiratory surfaces (Barthlolmew and Tucker, 1963; Bartholomew et al., 1965; Grigg and Alchin, 1976; Wood and Lenfant, 1976; Bartholomew, 1982). In the present study, not only were there no significant differences in heating rates between lizards that had previously dived and those that had not, but dead lizards after a “dive” heated as rapidly as living ones. Clearly, evaporative cooling either of the skin or the respiratory surfaces was negligible in its effect on heating rates under the experimental conditions of this study. Physiological thermoregulation of reptiles in air has been reviewed by Grigg and Alchin (1976) Jammes and Grimaud (1976), Smith (1976, 1979); Crawshaw (1979), Huey and Stevenson (1979), Bartholomew and Vleck (1979), Bartholomew (1982) and Heatwole and Taylor (1987). In general, reptiles heat more rapidly than they cool, particularly in humid air, and they exhibit higher heart rates, rates of oxygen consumption and ventilation frequencies during heating than during cooling. The increased heart rate is associated with greater peripheral blood flow enabling a more rapid heat transfer from the exterior to the body core. Metabolic heat production usually contributes a small but variable influence on the rate of heating, and is more important in larger reptiles. Larger animals possess a greater capacity for physiological thermoregulation than do smaller ones. However, exceptions exist for each of these generalizations. Some reptiles, especially very small ones, cool faster than they heat (Spray and May, 1972; Grigg ef al., 1979; Fraser and Grigg, 1984; Fraser, 1980), do not always change heart rate with body temperature (Jacob and McDonald, 1975), or do not alter ventilation frequency with change in body tem-
Heating and cooling of lizards
491
Table 5. The relationship between Tan values and body weight for small lizards (< 20 g) heating and cooling in air
Tau heating (min)
Tan cooling (min) Mean i_ SE
Mass (g) Mean + SE
N
Mean + SE
0.939 * 0.054
IO
4.129 f 0.302
L. guichenoti
I.189 kO.076
I5
3.744 * 0.194
3.206+0.119
L. mustelina
2.501 * 0.159
7
4.694 f
0.330
4. I80 + 0.349
4.979 & 0.274 8.33 k I .03 12.755 + I.155 13.31 * 0.95 18.37 i 0.98
IO 3 2 I5 I5
6. I89 + 5.44 k I I .OOi 8.56 + ll.27*
0.384 0.320 0.750 0.548 1.849
5.485 + 0.300 6.98 f 0.473 10.85 + 0.349 7.43 i 0.418 9.l5fO.285
Species Lampropholis
Ctenotus
delicata
taeniolatus
Sphenomorphus
S.
quoyii
(juveniles)
quoyii
(adults)
tympanum
Ctenotus
robustus
Sphenomorphus
3.238 + 0.196
Reference Fraser (1980) Fraser (I 980) Fraser ( 1980) Fraser (I 980) This Study Fraser (1980) This Study This Study
The regression equations are: Source This Study Gregg et al. (1979) Smith (1976) Gregg et al. (1979) Smith ct al. (1984)
Animals <2og “lizard shaped reptiles” > 100 g Alligators 6C-764 g “lizard shaped reptiles” > 100 g Alligators 37-103 kg
M = mass, in grams, in all studies except Smith
Medium
N
air air air water water
8 9 I3 9 22
Heating In 7 = I .29 + 0.35 In M In z = 0.72 + 0.36 In M In r = 0.415 + 0.328 In M In r = 2. I I + 0.61 In M r = 8.81 MO50
Cooling Inr=l.l3+0.39InM In r = 0.42 + 0.44 In M In r = 0.237 + 0.433 In M Inr = -2.07f0.66InM r = 12.61 Mo6’
et al. (1984) where M is in kg.
perature (Bennett, 1973; Snyder and Weathers, 1976). Moreover, some species exhibit elevated heart rates during heating which do not influence the rate of temperature change (Weathers and White 1971; Lucey 1974). S. quoyii and Ctenotus both exhibit physiological thermoregulatory responses that differ from the general pattern in two ways: (1) their heart rate and ventilatory responses are ineffective in controlling heating and cooling rates and (2) they cool faster than they heat. These will be discussed in turn. S. quoyii and C. robustus exhibited higher heart rates and breathing rates during heating than during cooling (Daniels et al., 1987) but cooled faster than they heated. Moreover, dead lizards heated and cooled at the same rate as living ones. Such a response negates the hypothesis that increases in heart and breathing rates affect the thermoregulatory process. Heart rate may increase during heating, thereby maintaining blood pressure which otherwise would decrease in response to peripheral vasodilation (White, 1976). Cooling may stimulate cutaneous vasoconstriction which also may reflexly affect blood pressure. The function of the differences in ventilation rates is unknown, but may reflect differences in oxygen consumption. Bartholomew and Vleck (1979) observed Amblyrhynchus cristatus to consume more oxygen during heating than during cooling, but this remains to be verified for smaller lizards. Both S. quoyii and C. robustus cooled faster than they heated. The trends in heating and cooling may be related to body size. If the 5 values for heating and cooling are regressed against body size for lizardshaped reptiles larger than 100 g (Grigg et al., 1979) or alligators larger than 60 g (Smith, 1976) (Table 4), as body mass decreases, both reveal relatively smaller 7 values during heating than during cooling. The regressions intersect (7 heating = 7 cooling) at a body weight of 46 g using the equations of Grigg et al. (1979) and at one of 42 g using that of Smith (1976). Using our data on S. quoyii and C. robustus and the 5 values for several other small skinks (Fraser, 1980; Fraser and Grigg, 1984) the regression lines intersect at 48 g (Table 5). These results consistently predict that lizards smaller than 40-5Og should cool faster than they heat. It has often been argued that the
ability to heat faster than cool is advantageous and under physiological control, but that the converse represents the absence of any physiological capacity to control body temperature (Bartholomew, 1982). However, very small, dead lizards heat and cool at the same rate (Fraser, 1980; Table 5). Hence the ability to cool faster than heat, may be under some physiological control. The nature of such physiological processes still remains to be determined. Acknowledgements-We are grateful to the Commonwealth Postgraduate Scholarship Fund for financial support (to
C.B.D.). Sandra Higgins typed the manuscript, Lynda Bridges prepared the figure and Maria McCoy and Russell Hobbs provided technical assistance and help with the computing. REFERENCES
Bartholomew G. A. (1982) Physiological control of body temperature. In Biology of rhe Reptilia (Edited by Gans C. and Pugh F. H.), Vol. 12, pp. 167-212. Academic Press, London. Bartholomew G. A. and Tucker V. A. (1963) Control of changes in body temperature, metabolism and circulation by the agamid lizard Amphibolurus barbatus. Physiol. Zool. 36, 199-218. Bartholomew G. A., Tucker V. A. and Lee A. K. (1965) Oxygen consumption, thermal conductance and heart rate in the Australian Skink Tiliqua scincoides. Copeia 1%5, 169-173.
Bartholomew, G. A. and Vleck D. (1979) The relation of oxygen consumption to body size and to heating and cooling in the Galapagos marine iguana Amblyrhynchus crisfatus. J. camp. Physiol. 132, 285-288.
Bennett A. F. (1973) Ventilation in two species of lizards during rest and activity. Camp. Biochem. Physiol. 46A, 653-67 1. Cogger H. G. (1979) Reptiles and Amphibians of Australia, 2nd edn. Reed, Sydney. Crawshaw L. I. (1979) Responses to rapid temperature change in vertebrate ectotherms. Am. Zool. 19, 225-237. Crisp M., Cook L. M. and Hereward F. V. (1979) Colour
and heat balance in the lizard Lucerta dugesii. Copeia 1979, 250-257.
Daniels C. B. (1984) The adaptations to a riparian habitat by the water skink Sphenomorphus quoyii. Ph.D. Thesis, University of New England. Daniels C. B., Oakes N. and Heatwole H. (1987) Physiological diving adaptations of the Australian water
492
CHRISTOPHERB.
skink, Sphenomorphus auovii. Comp. Biochem. Physiol. A (in press).
Fraser S. P. (1980) Insights into the physiological and behavioural thermoregulatory abilities of small lizards. B.Sc.(Hons) Thesis, University of Sydney. Fraser S. P. and Grirrg G. C. (1984) Control of thermal conductance is ins@ficant td ther~oregulation in small reptiles. P~~~io~~Zool. 57, 392400. Grigg G. C. (1976) Practical notes and comments on the application of X, the thermal time constant, to analysis of responses by reptiles to step function increases or decreases in ambient temperature. University of Queensland, Department of Zoology Practical Notes, Brisbane, Queensland. Grigg G. C. and Alchin J. (1976) The role of the cardiovascular system in the thermoregulation of Crocodylus johnstoni. Zoology 49, 24-36. Grigg G. C., Drane R. and Courtice G. P. (1979) Time constants of heating and cooling in the eastern water dragon Physignathus Iesueurii and some generalizations about heating and cooling in reptiles, J. Therm. Biol. 4, 95-103.
Heatwoie H. (1976) Repfjle Ecology. University of Queensland Press, St. Lucia. Heatwole H. and Taylor J. (1987) Ecology of Reptiles. University of Queensland Press, St. Lucia. (In press). Huey R. 8. and Stevenson R. D. (1979) Integrating thermal p~ysioIogy and ecology of ectotherms. A discussion of armroaches. Am. Zool. 19, 357-366. Jacob J. S. and McDonald H. S. (1975) Diving bradycardia in four species of North American aquatic snakes. Comp. Biochem. Physiol. 53A, 69-72.
DANIELSet al. Jammes Y. and Grimaud C. (1976) Ventilation, pulmonary and cutaneous gas exchange in the awake lizards Lucerra airi& Camp. Biochem. Physiol. !%A, 279-285. Lucey E. C. (1974) Heart rates and physiological thermoregulation in a basking turtle Psuedemys scripta elegans. Comp. Biochem. Physiol. 48A, 471482. Smith E. N. (1976) Heating and cooling rates of the American alligator, AIIigutor m~s~ss~ppiensis, Physiol. ZOOI. 49, 37-48.
Smith E. N. (1979) Behavioural and physiological thermoregulation of crocodilians. Am. 2001. 19, 239-247. Smith E. N., Standora E. A. and Robertson S. L. (1984) Physiological thermoregulation of mature alligators. Comu. Biochem. Phvsiol. 77A, 189--193.
Snyder. G. K. and Weathers W. W. (1976) Physiological responses to temperature in the tropical lizard Hemidactylus~enatus (Sauria: Gekkonidae). Herpetologica 32, 252-256. Sokal R. R. and Rohlf F. J. (1969) Introduction to Biosfatistics. W. H. Freeman and Co., San Francisco. Spray D. C. and May M. L. (1972) Heating and cooling rates in four species of turtles. Comp. Biochem. PItysiol. 41 A, 507-522.
Weathers W. W. and White F. N. (1971) Physiological thermoregulation in turtles. Am. I. Physiol. 221,704710. White F. N. (1976) Circulation. In Biology of the Reptilia (Edited by Gans C. and Dawson W. R.), Vol. 5, pp. 275-334. Academic Press. London. Wood S. C. and Lenfant C. J. M. (1976) Respiration: Mechanics, control and gas exchange. In BioIogy of the Reptilia (Edited by Gans C. and Dawson W. R.), Vol. 5, pp. 225-274. Academic Press, London.