Physiological diving adaptations of the australian water skink Sphenomorphus quoyii

0300-9629/87 $3.00 + 0.00 0 1987 Pergamon Journals Ltd

Camp. Biochem. Physiol. Vol. 88A, No. 2, pp. 187-199, 1987

Printed in Great Britain

PHYSIOLOGICAL DIVING ADAPTATIONS OF THE AUSTRALIAN WATER SKINK SPHENOMORPHUS QUO YH CHRISTOPHER B. DANIEL&*NICHOLASOAKENand HAROLDHEATWOLE Department of Zoology, University of New England, Armidale, N.S.W. 2351,Australia and *Department of Physiology, School of Medicine, Flinders University of South Australia, Bedford Park, S.A. 5042, Australia (Received 14 January 1987) Abstract-l. Both the small riparian skink Sphenomorphus quoyii and its completely terrestrial relative Crenorus robustus respond to forced submergence with instantaneous bradycardia. 2. The strength of the bradycardia was affected by water temperature and fear. Dives into hot (30°C) water produced weak and erratic bradycardia compared to dives into cold (19.5”C) water. For S. quoyii the strongest bradycardia occurred when submergence took place in water at a lower temperature than the pre-dive body temperature. 3. Upon emergence both species of skink exhibited elevated heart rates and breathing rates while heating from 19.5 to 30°C compared to heating at rest. The increased heart and breathing rates probably act to replenish depleted oxygen stores and remove any lactate. Increased heart and ventilation rates are not indicators of physiological thermoregulation in this case. 4. Both lizard species exhibited higher heart rates and ventilation frequencies during heating than cooling. 5. Compared to its terrestrial relative, S. quoyii does not appear to possess any major thermoregulatory, ventilatory or cardiovascular adaptations to diving. However, very small reptiles may be generally preadapted to use the water to avoid predators.

INTRODUCTION Studies of reptilian diving physiology are numerous and are summarized in general treatments by Heatwole and Seymour (1976), Butler and Jones (1982) and Seymour (1982). In addition, there have been reviews of the specific role of cardiovascular (White, 1976, 1978; Avery, 1982; Bartholomew, 1982; Huey, 1982) and respiratory (Bennett and Dawson, 1976; Wood and Lenfant, 1976; Pough, 1979; Glass and Wood, 1983) processes. Small reptiles, because of their greater surface area to volume ratios, would be expected to have quantitatively, if not qualitatively, different respiratory and cardiovascular responses during diving, than would larger ones. Interest in reptilian diving physiology has centered on the larger diving species and small diving forms have been poorly or incompletely studied. The aim of the present study was to expand the size range of the comparative base by exploring some aspects of the diving physiology of the small, semi-aquatic scincid lizard, Sphenomorphus quoyii and compare its properties with those of its completely terrestrial relative Cfenotus robustus. Heart and ventilation rates before, during, and after diving were examined. MATERIALSAND METHODS Lizards were collected by hand in January 1983, water skinks (Sphenomorphus quoyii) from the edges of creeks in the vicinity of Armidale, N.S.W. and robust skinks (Crenotus robustus) from adjacent terrestrial habitats. They were maintained in the laboratory in tanks appropriate to their respective natural habitats (for details see Daniel% 1984).

For at least a week prior to experimentation lizards were maintained on a 12L: 12D photoperiod with day-time mmperatures of 2326°C and nocturnal ones of l&lY’C. They were fed during the experiments. Fifteen C. robustus (87.3 f 1.97mm.SVL; 1313+ 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 f 3.05 mm SVL; 8.3 f 1.03 g) were used. Heart rate

For experimental purposes, a lizard was selected and cold-anaesthetized by placing it in chipped ice. Then, three E2B subdermal electroneedles were inserted beneath the skin on the ventral surface. The recording electrodes were placed laterally to the heart and the earth lead was inserted in the base of the tail. All were held in place with small drops of liquid adhesive. Heart beats and breaths were recorded using a Grass model 7D polygraph recorder (Mullen, 1967; Jacob and McDonald, 1975). The experiment proceeded in seven stages which were always undertaken in the same order. (1) The cold lizard was placed in the tube which was put into a water bath at 30.6 f 0.32”C (termed a 30°C water bath) until body temperature (Ta) reached 30°C. (2) The lizard was maintained at that body temperature for 5 min. (3) The tube containing the lizard was removed from the 30°C water bath and placed in an adjacent water bath at 19.4 f 0.17”C (termed the 19.5”C water bath). One stopper was removed and the tube flooded with water. The lizard remained submerged for 12 mm, a time representing twice the mean voluntary diving time, at 195°C (Daniels, 1984). (4) At the conclusion of thi “12mm dive” the lizard was removed from the 19.5” bath. the tube drained of water and the stopper replaced. The animal, breathing freely, was then placed, in its tube, in the 30°C bath until it had regained a body temperature of 30°C. (5) The lizard was maintained at 30°C Ts for 5 min. (6) The lizard in the air-filled tube was transferred to the 19.5”C bath and cooled until its body temperature was identical to 187

CHRISTOPHER B. DANIELSet al.

188

that reached at the conclusion of diving (usually between 20 and 20.5”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, each animal was heated in air, cooled submerged in water, reheated in air, cooled in air, and heated in air once more; they were 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 (Pidgeon, 1978) during the active season of the lizards; furthermore, 30°C is similar to the preferred body temperature of S. quoyii (Heatwole, 1976). The experimental design incorporates four assumptions: (1) that one stage was not affected by any preceeding stage, or by the order of the experimental stages, except for heating after a dive; (2) that the presence of the experimenters and the transfer of lizards between water baths did not affect heart rates or breathing rates; (3) that lizards did not exhibit changes in heart rate or breathing rate over time as a result of the long incarceration in the tube; (4) that the results were repeatable on any individual. Tests of these assumptions were made by Daniels (1984). It was found that only the first assumption was completely valid, but departures from the other three were slight and probably had little effect on the data. Hence, they are accepted as true for the purposes of the present experiments. Heart rates and breathing rates were recorded continuously throughout all stages. Body temperature was recorded every 15 sec. To correlate heart and breathing rates with body temperature, the beats and the breaths occurring in the 7 set before and after the time of the temperature readings were counted and the values over 14sec were converted to beats or breaths per min. This method eliminated any overlap in the heart or breathing rates between two successive temperatures. Several additional experiments were also undertaken. The heart rates and breathing rates of adult lizards diving at constant temperatures were measured on six S. quoyii and three C. robustus. They were cooled in the 19.5”C bath and maintained at that temperature for lOmin, then the tube was flooded for 12min. One “dive” was conducted per lizard. Similarly, lizards were warmed to 3O”C, maintained at that temperature for 10 min and then the tubes flooded. Because the lizards appeared to experience discomfort at the end of a 12-min dive at 3o”C, these dives were shortened to 8 min. Heart and breathing rates were calculated at each half degree between 20 and 30°C in each stage for all three groups (C. robustus,adult S. quoyii,juvenile S. quoyii) and regression analyses performed on the mean values at each temperature. Linear and natural logarithmic regressions

were performed. Differences between species or size groups at any stage and differences between stages for any species or size group were determined using one-way analysis of covariance on the natural logarithms of the mean values (Snedecor and Cochrane, 1978). Although logarithmic regression may not always best describe relationships (e.g. some breathing rates) they represent the best transformation for analysis. Most regressions were plotted semilogarithmically. However, some figures, particularly those with data from all three animal groups, were plotted on linear scales. In these cases, the mean values were plotted and the logarithmic regressions fitted. RESULTS Heart rate

Prior to diving, C. robustus exhibited higher heart rates at 30°C than did juvenile S. quoyii which in turn had values slightly higher than those of adult S. quoyii (Table 1). Almost immediately upon submergence all lizards exhibited a strong bradycardia with heart rate decreasing to between 10 and 30 beats per min which was maintained throughout the dive (Fig. 1). Adult S. quoyii exhibited significantly lower diving heart rates than did juveniles, which in turn had lower ones than did C. robustus (F2, ,39= 131.45, P < 0.05; Fig. 1). Both S. quoyii and C. robustus exhibited bradycardia if diving into either hot (30°C) or cold (19.YC) water compared to the resting state (Figs 2, 3, 4 and 5). However, both lizard species exhibited higher and more erratic heart rates while diving in hot water than in cold water (Figs 2, 3, 4 and 5). Sphenomorphus and Ctenotus appeared to exhibit the strongest bradycardia with the lowest variability when there was a temperature gradient associated with the submergence (Figs 6 and 7). S. quoyii exhibited its strongest and most consistent bradycardia when diving from 30°C air into 19.5”C water (Fig. 6). Heart rates were higher for lizards diving with a T, of 19.5”C into 19.5”C water, and were high and erratic during the 30°C dives (Fig. 6). These heart rates differed significantly (FL 125 = 274.12, P < 0.05). C. robustus with a TB of 19.5”C diving into water of the same temperature exhibited the strongest initial bradycardia. However, the lizards diving form 30°C air into 19.5”C water exhibited lower heart rates in the latter portion of the dives and maintained a more consistent heart rate (Fig. 7). C. robustus diving at

Table I. One-way analysis of variance for the heart rate of adult and juvenile Sphenomorphus and adult Ctenorus ro6u.rrus at 30°C

quoyii

Prior to diving

Heart rate Group S. quoyii adults S. quoyii juveniles C. robustus

(beats/min)

N

93.93 f 5.13 95.73 * 5.17 121.29 rfr4.65

12 3 10

ss Treatments Error Total

4380.70 5576.42 9957.12

ANOVA d.f. MS 2 22 24

2190.35 253.47

Table F

P

8.64

<0.05

Prior to cooling

Heart rate Group S. quoyii adults S. quoyii juveniles C. robustus

(beats/min)

N

100.18 k 9.96 108.6 + 5.70 126.86 f 8.89

8 3 10

ss Treatments Error Total

3270. I2 9058.40 12,328.57

ANOVA d.f. MS 2 18 20

1635.08 503.24

Table F

P

3.25

>O.OJ

Measurementswere undertaken prior to diving and again prior lo the heating and cooling experiments. Heart rate expressed as means f SE.

Diving adaptations of small lizards

189

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2 E

60-

1

50-

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Sph6nomorphus quoyii adults

O---O

Sphenomorphus quoyii juveniles

o-

Ctenotus robustus

F i? & 40P 30-

20-

IO-

0-

d

i

1

4

1

!i TIME

$

UNDERWATER

f

‘ii

b

lb

li

li

(min.)

Fig. 1. Heart rates regressed against time underwater for lizards diving from Ts = 30°C into 19.5”C water for 12 min. The regression equations are: adult Sphenornorphus quoyii, y = -4.80 In x + 21.89, N = 48, r2 = 0.69, juvenile Sphenomorphus quoyii, y = -4.80 In x + 21.89, N = 48, r2 = 0.49, Cienotus robusfus, y = - 5.24 In x + 35.57, N = 48, r2 = 0.58. Vertical lines represent standard errors, numbers with symbols are sample sizes.

0

I

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I

I

2

3

4

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6 5 TIME (mln.1

I

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7

e

9

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II

Fig. 2. Heart rates of Sphenomorphus quoyii resting and diving at 19.5% The regression equations are: resting, y = 5.90 In x + 59.76, N = 48, r2 = 0.53; diving, y = 5.67 In x + 28.08, N = 48, r2 = 0.83. Symbols as in Fig. 1.

I I2

CHRISTOPHER

190

B. DANIELSet al.

so c) .f

E fi

60

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70

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w I SO

40

30

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0

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I 2

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3

I 4

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5

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TIME (min.)

Fig. 3. Heart rates of adult Sphenomorphus quoyii resting and diving at 30°C. Symbols as in Fig. 1.

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2

3

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(min.)

Fig. 4. Heart rates of adult Ctenorus robustus resting and diving at 19S”C. The regression equations are: resting, y = -0.26 In x + 52.25, N = 48, r* = 0.28; diving, y = -0.27 In x + 25.04, N = 48, r2 = 0.00426. Symbols as in Fig. 1.

I I2

Diving adaptations of small lizards

191

2 30-

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, 5

, 4

I 3

I 2

I I

, 6

I 7

I 6

TIME fmin.) Fig. 5. Heart rates of adult Crenotus robustas resting and diving at 30°C. The regrassion equations are: resting, y = -0.84Inx+79.84, N=32, r*=0.20; diving, y= -61ln.x+60.54, N=29, rZ=o.52. Symbols as in Fig. 1.

loo

1

90

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70

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TO 19+5”C

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8

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UNDERWATER

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12

(min.)

Fig. 6. Heart rates of adult Sphenomorpkus quoyii diving at different temperatures. The regression equations are: 30°C y = -2.35 In x + 40.48, N = 32, r* = 0.32; 19S”C, y = -5.67 In x + 28.08, N = 48, r2 = 0.83; 30-19YC, y = -4.80 In x + 21.89, N = 48, r2 = 0.69. Symbols as in Fig. 1.

CHRISTOPHER B. DANIELS et ai.

I92

2

a-0

Diving at 30%

o-

Diving at 19.5’C

A-A

Diving from 30% to lS~!!i*C

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8

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(min.f

Fig. 7. Heart rates of adult Ctenorus robustus diving at different temperatures. The regression equations are: 3O”C,y = -6.6 in x + 60.54, N = 29, r2 = 0.32; 19.5”C,y = 0.27 In x + 25.04, N = 48, r2 = 0.00426, 30-19.5”C, y = -5.24Inx+35.37, N=48, r”=O.S8. Symbolsas in Fig. 1. 30°C exhibited a poor and erratic bradycardia (Fig. 7; Fz 122 = 397.81, P < 0.05). It seems, therefore, that

there are two components to diving bradycardia: an effect directly associated with the submergence and a thermal effect. The former accounts for most of the decrease in heart rate (Figs 6 and 7).

When heating after the termination of the dive all groups exhibited an increase in heart rate with increasing body temperature (Fig. 8). The heart rates of C. robustus were significantly higher at any body temperature than those of adult or juvenile S. quoyii during this stage (F2,5, = 82.98, P -c 0.05; Fig. 8).

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o--o

Ctenotus robustus

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+A

Sphenomorphus

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IIO-

o-----El

Sphenomorphus quoyii juveniles

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80-

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adults

7060SO4030r 20

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22

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f

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23

24

25

26

27

28

29

BODY

TEMPERATURE

1 30

(“C)

Fig. 8. Heart rates regressed against body temperature for lizards heating from 19.5 to 30°C immediately after a dive. The regression equations are: adult Sphenomorphus quoyii, y = 104.3 In x - 260.23, N = 20, r* =0.98, Q ,,, = 1.713; juvenile Sphenontorphus quoyii, y = 172.8 In x - 471.69, N = 18, r2 = 0.97, Q,, = 1.624; Ctenorus robustus, y = 178.16 In x - 478.21, n = 20, rz = 0.99, Q,, = 2.084. Symbols as in Fig. 1.

Diving adaptations of small lizards

E F 2 8 8 E

120-

o-o

ctenotlls robustus

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Sphenomorphus

quoyii adults

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Sphenomorphus

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193

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22

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25

26

27

28

29

30

1

23 BODY

TEMPERATURE

(Oc)

Fig. 9. Heart rates regressed against body temperature for lizards cooling from 30 to 195°C. regression equations are: adult Sphenomorphus quoyii, y = 131.29 In x - 362.59, N = 20, r2 = Q,, = 2.507; juvenile Sphenomorphus quoyii, y = 152.5 In x - 420.14, N = 19, r2 = 0.98, Q,, = Crenorus robustus, y = 158.32 In x - 422.36, N = 20, r2 = 0.99, Q,, = 2.166. Symbols as in Fig.

C. robustus exhibited the highest heart rate at 30°C after this heating period (Table 1). Although all three groups exhibited higher heart rates at 30°C after the dive than before it, these differences were not significant (S. quoyii adults, t = 0.88, d.f. = 7, P > 0.05; S. quoyii juveniles, t = 3.00, d.f. = 2, P >0.05; C. robustus, t =0.57, d.f. = 9, P > 0.05; Table 1).

The 0.97, 3.38; 1.

During cooling, heart rate decreased with body temperature. C. robustus exhibited significantly higher heart rates than did juvenile S. quoyii, which in turn had higher ones than adults of that species (F2,57= 312.49, P < 0.05; Fig. 9). Heart rates increased with body temperature during the heating stage. Heart rates were highest for juvenile S. quoyii and lowest for adult S. quoyii at any temperature

120-

IIO-

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o-o

Ctenotus robustus

A-A

Sphenomorphus

O-•rl

Sphenomorphus quoyli

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20

1

21

juveniles

I

22

I

23

24 BODY

Fig. 10. Heart rates regression equations Q,, = 1.934; juvenile Ctenotus robustus,

adults

quoyii

25

TEMPERATURE

26

27

,

28

29

30

(“C)

regressed against body temperature for lizards heating from 19.5 to 30°C. The are: adult Sphenomorphus quoyii, y = 93.16 In x - 233.6, N = 20, r2 = 0.91, Sphenomorphus quoyii, y = 90.65 In x - 203.6, N = 20, r2 = 0.96, Q,, = 1.520; r = 117.73Inx -296.0, N =20, r2=0.96, Q,,= 1.770. Symbols as in Fig. 1.

194

CHRISTOPHER B. DANIEU et al. Table 2. One-way analysis of variance for the breathing rate of adult Sphenomorphur quoyii and adult Ctenotus robustus at 30°C Prior to diving Group S. quoyii C. robust&s

Breathing rate (breathslmin)

N

32.0k2.1 42.4 + 1.6

11 10

ss Treatments Error Total

575.90 729.03 1304.93

ANOVA d.f. MS 1 19 20

575.90 38.37

Table F

P

IS.01

-co.05

Prior to cooling Grou” S. quoyii C. robustus

Breathing rate (breathsiminj 33.7 * 1.7 42.9 k 3.3

N 7 9

ss Treatments Error Total

331.09 933.49 1264.58

ANOVA d.f. MS 1 14 15

331.09 66.68

Table F

P

4.97

to.05

Measurements were undertaken urior to diving and again prior to the heating and cooling experiments. Breathing rate expressed as means f SE. -

during this stage (F,,,, = 187.35, P ~0.05; Fig. 10). Thus in each experimental stage C. robustus exhibited the greatest heart rates at any body temperature, with adult S. quoyii exhibiting the lowest. Juvenile S. quoyii had the smallest heart rate Q,, during the heating stages and the largest during the cooling stage. Adult S. quoyii and Ctenotus had similar Q,, at all stages. Adult water skinks exhibited significantly greater heart rates when cooling at rest than during the dive (Fi,j, = 128.15, P < 0.05). They also exhibited higher heart rates during heating than during cooling (F,. 138= 31.93, P < 0.05). Also, heart rates were significantly greater for the adults after the dive than when heating at rest (F,.,, = 172.79, P < 0.05). Similar significant differences were observed for the juvenile S. quoyii and Ctenotus. For all groups, heart rate Q,, was greater during cooling then during heating and, except for the adult water skinks, Q,, was greater when heating after a dive than when heating at rest. Breathing rate

At the commencement of the experiments and after heating after the dive, C. robustus had a significantly higher breathing rate at 30°C than did S. quoyii (Table 2). However, there were no significant intraspecific differences in breathing rates at 30°C before and after the dive (C. robustus, t = 0.34, d.f. = 9, P > 0.05; S. quoyii, t =0.59, d.f. = 5, P > 0.05). Breathing rates increased with Tt, for both species and C. robustus maintained significantly higher breathing rates and lower Q,, than did S. quoyii in all the experiments of heating after a dive, and cooling and heating at rest. Thus for heating after a dive, S. quoyii breathing rate was y = 27.98 In x - 61.29, r2 = 0.84, N = 20; C. robustus, y = 29.841 In x - 59.85, r2 = 0.76, N = 20; F,,,, = 193.67, P < 0.05. Cooling: S. quoyii, y = 32.51 In x - 85.31, r2 = 0 85 N = 20; C. robustus, y = 55.48 In x - 151.20, r2 = 0.79, N = 20; F,,,, = 142.77, P < 0.05. Heating at rest: S. quoyii, y = 35.31 In x - 88.89, r2 = 0.78, N = 20; C. robustus, y = 35.10 In x -81.40, r2=0.89, N=20; F,,,,= 119.45, P < 0.05). Adult S. quoyii and C. robustus both had significantly higher breathing rates and lower Q,, during heating than during cooling, and during heating after a dive than when heating at rest, at any body

temperature.

The Q,, for breathing rate of adult S.

quoyii were: heating after a dive 1.327; cooling 2.165; heating at rest 2.028. For C. robustus they were:

heating after a dive 0.792; cooling 1.928; heating at rest 1.537. DISCUSSION

Reptiles show increases in both heart rate and breathing rate with decreasing body mass (Tables 3 and 4). Both S. quoyii and C. robustus had heart rates and breathing rates equivalent to those of other lizards with a similar body mass, and similar to those predicted from regression equations for saurian species between 13 and 20 g (Tables 3 and 4). Intraspecifically, there is also an increase in heart rate with decreasing body size, with juvenile S. quoyii exhibiting greater heart rates at 30°C than did adults. S. quoyii and C. robustus exhibited high rates of breathing and heart beat at 30°C prior to the commencement of the experiment (Tables 3 and 4). Heart rates (and possibly rates of ventilation) may become elevated in response to an unaccustomed situation (Huggins et al., 1969). A slight heart rate decrease over time was observed for both species if left in the tube at 30°C for 2 hr (Daniels, 1984) and similar heart rate decreases have been observed for other reptiles (Gaunt and Gans, 1969; Huggins et al., 1969; White, 1976). Moreover, reptiles may either increase (Huggins et al., 1969; Gaunt and Gans, 1969) or decrease (Belkin, 1968) their heart rates in response to the presence of investigators, with either change frequently being accompanied by apnea (SchmidtNielsen et al., 1966). Activity may also greatly increase both heart rates and breathing rates (Licht, 1965; Huggins et al., 1969; Heatwole, 1975, 1977; White, 1976), although Bennett (1973) did not observe changes in ventilation rate after activity for several species of lizards. McDonald and Heath (1971) also found that the restraint necessary for affixing the ECG leads was a significant factor in elevating heart rates in tuataras. Diving

White (1976) and Seymour (1982) summarized the extensive literature on the cardiovascular responses to diving and concluded that forced dives are usually accompanied by severe bradycardia, increased per-

Diving adaptations of small lizards Table 3. The relationship

between heart rate and body wt for lizards at 30°C Heart rate (beatslmin)

Species

Sceloporu~ graciouFus Sphenomorphus

quoyii

90 95.7 121.3 93.9 90 40 40 40 50 30 45 50 40 46 50 43 57.5 35 63 45

(juveniles)

Crenorus robustus Sphenomorphus

Uma

quoyii

(adults)

notata

Dipsosaurus Tiliqua

dorsalis

rugosa

Sauromalus

obesus

Ctenosaura

hemilopa

Tiliqua

rugosa

Egernia

cunninghami

Sauromalur

obese

Amphibolurus Tiliqua

tumidus

barbatus

scincoides

Physignathur

lesueurii

Amblyrhynchus Iguana

cristatus*

iguana

Amblyrhynchus Iguana

cristatus

iguana t

Varanw

195

niloticus

Body wt (9) 7.4 a.37 13.31 18.37 19.2 70.4

100 150 164 257 266 300 373 496 560 652 1050 1800 3000 4800

Reference Licht (1965) This study This study This study Licht (1965) Licht (1965) Licht (1965) Boyer (1967) Weathers and Morgareidge (1971) Wilson (I 974) Wilson (1974) Templeton (1964) Bartholomew and Tucker (1963) Bartholomew et al. (1965) Wilson (1974) Bartholomew and Lasiewski (1965) Tucker (1966) Morgareidge and White (1969) Baker and White (1970) Wood and Johansen (1974)

Heart rates are those of resting animals at equilibrium with environmental temperatures. When wt ranges are given, the largest wts are selected. Regression equation: HR = 113.83~ m0.‘4.N = 20, r2 = 0.49. Bartholomew and Tucker’s (1964) regression for varanids is: HR = 87.1~~ m”.‘sJ. ‘T, = 26°C. tTB = 29.2”C.

ipheral resistance, muscle ischaemia and anaerobic metabolism. Right-to-left intraventricular shunting increases and can lead to a complete pulmonary bypass (see also Jackson and Silverblatt, 1974; Seymour and Webster, 1975; Irvine and Prange, 1976). The physiological responses occurring during forced dives, or those undertaken to escape predators, differ considerably from those of voluntary dives for feeding or other underwater activities (Huggins et al., 1969; Wood and Johansen, 1974; Heatwole, 1977). However, some escape dives do not exhibit a great bradycardia (Courtice, 1981a, b). Diving bradycardia appears to be mediated by the parasympathetic system (Belkin, 1964; White and Ross, 1965; Huggins ez al., 1969; White, 1970, 1976; Butler and Jones, 1982) and is usually due to an elongation of ventricular diastole (Johansen, 1959; Anderson, 1961). Stroke volume probably increases greatly. In some species bradycardia can be elicited by water on the nostrils (Johansen, 1959) and may be accentuated by water immersion or the concomitant increase in hydrostatic pressure (Anderson, 196 1; Berkson, 1966; Seymour, 1978). Both S. quoyii and C. robustus appear to exhibit some of the physiological characteristics associated with forced dives, when they are submerged. The strength of the bradycardia may be affected by

Table 4. Ventilation Species Seineella

laterale

Xanturia

vigilis

Hemidactylur Sceloporus Ctenotus Uta

38

frettams occidentalis

robustus

mearnsi

Sphenomorphus

Lacerto

freouencies

Ventilation frequency (breaths/min)

quoyii

sp.

Bennett’s (1973) relationship N= 16.

two factors; submergence and water temperature. S. as a means of escaping predators, a fear-inducing situation. Consequently, fearbradycardia may accompany submergence in water at any temperature, instituting the physiological changes listed above. However, if fear were the only factor affecting the degree of bradycardia, then consistent heart rates would be predicted for lizards diving at different water temperatures or with different initial 7’a. Such is not the case for either S. quoyii or C. robustus or for many anurans (Butler and Jones, 1982). It is hypothesized that environmental temperature may affect bradycardia in the following manner: Diving elicits parasympathetically mediated changes in the cardiovascular system that include peripheral vasoconstriction, right-to-left heat shunts and a decrease in heart rate. However, cold also stimulates peripheral vasoconstriction independently of the neural response (Morgareidge and White, 1969; Baker et al., 1971; White, 1976). The increased peripheral vasoconstriction may increase fluid pressure in the major vessels thereby reducing the frequency of heart beats necessary to maintain blood pressure at an optimum level. The lower temperature decreases metabolic rate, thereby enabling the ischaemic tissue to respire anaerobically for longer quoyii dives primarily

of small lizards I < 30 a1 at 30°C Body wt (g) 1.0

5

1.1

25

4.4

35

12.8

42.4

13.31

19

14

32

18.37

38 of breathing

19

Reference Hudson and Bertram (1966) Snyder (1971a) Snyder and Weathers (1976) Francis and Brooks (1968) This study Murrish and Vance (1968) This study Nielsen (1961a, b)

rate to body mass in lizards at 30°C isf=

12.8 W-O”, r = -0.23,

196

CHRISTOPHER B. DANIEL.V et al.

periods and reduce the demand for oxygen during the dive. Moreover, cold may influence the parasympathetic system directly to further reduce the heart rate (Butler and Jones, 1982). Cold increases the vagal effects on isolated toad hearts (Courtice, pers. comm.). The high specific heat of water coupled with the large surface area to volume ratio of these small skinks enables the temperature effects to be rapidly conducted to the body core. With reptiles acclimated at low temperatures there may be a certain amount of red blood cell sequestration in the spleen, skin, muscle, kidney and gut (Anderson, 1961; Snyder, 1971b; Stitt and Semple, 1971) which would reduce the blood viscosity and further reduce the work of the heart. A third possibility is that the thermal shock of plunging into cold water may also enhance the fear response to submergence. At higher water temperatures, the physiological responses to fear and heat may oppose each other. Vasodilation in response to heating may decrease peripheral resistance and decrease the effectiveness of the vagal control over circulation (White, 1970, 1976). The increased metabolic rate decreases the time for which peripheral tissues can sustain anaerobic respiration and also promotes rapid oxygen utilization by those tissues still respiring aerobically. Moreover, the greater rate of CO2 production increases skin perfusion (Courtice, 1981c), further reducing peripheral vasoconstriction. Thus, the fear-bradycardia may be rapidly overridden by the physiological responses to high temperature, resulting in high and erratic heart rates. The temperature-mediated changes in diving physiology may also explain why voluntary diving time decreases with increasing water temperature (Daniels, 1984). In summary, this hypothesis suggests that small skinks with a high body temperature, forced or stimulated to dive into cold water, exhibit an immediate fearinduced bradycardia. The bradycardia is augmented and possibly maintained by the effect of cold which promotes peripheral vasoconstriction, decreases metabolic rate, and may increase vagal responses. Cold may reduce underwater activity; however, a true diving bradycardia is usually unaffected by activity (Pough, 1973; Heatwole, 1977; Baeyens et al., 1980; Seymour, 1982). The strength of the bradycardia observed in forced dives may not easily enable oxygen stored in the lung or blood to be transported to the essential organs. Bradycardia is often associated with a right-to-left intraventricular shunt and blood flow to the lungs may be greatly reduced. The cardiac shunt could reduce access to lung stores of oxygen while the low heart rate could reduce the effectiveness of the distribution of oxygen to the tissues. Many reptiles do not utilize all their lung oxygen when submerged (Seymour et al., 1981), although the lung oxygen reserves of the escape divers Varanus niloticus and Amblyrhynchus cristatus are usually extensively utilized (Wood and Johansen, 1974; Bartholomew et al., 1976). It may be hypothesized that, except for those tissues without a blood flow and which respire anaerobically, oxygen is provided to the tissues mainly from the blood. S. quoyii blood has a low oxygen affinity with the P, of adults ranging between 50 and 60 Torr (Grigg and Harlow, 1981). Thus, complete oxygen saturation of the blood rarely occurs but

oxygen is readily provided to the tissues at high partial pressures (Grigg and Harlow, 1981). Other blood characteristics of S. quoyii are not very different from those of other lizard species (Pough, 1979). Snyder (1971b) suggested that the oxygen carrying capacity increases with haematocrit. If S. quoyii either stores CO* in the tissues (Glass and Wood, 1983) or excretes the gas cutaneously, as do many other reptiles (Girgis, 1961; Graham, 1974; Jammes and Grimaud, 1976; Courtice, 1981~; Seymour, 1982), then the blood may be capable of supplying enough oxygen to sustain the essential organs during 12 min dives in cold water. Heating and cooling

During diving heat was removed from the lizard 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 were probably only small convectional air currents in the experimental chamber. Under these conditions S. quoyii and C. robustus heat at the same rate after the dive as they heated at rest (Daniels et al., in press). However, they both exhibited higher breathing rates during heating in the former condition. It was surprising to observe the equivalent rates of heating after the dive and heating at rest (Daniels et al., in press). The lizards were wet and some of the initial heat should be necessary to evaporate the water from the body surface. This evaporation could be predicted to reduce the rate of heating of the lizard. Moreover, increased rates of ventilation have frequently been associated with decreased heating rates because high ventilation rates are often associated with evaporative cooling (e.g. Bartholomew and Tucker, 1963; Bartholomew et al., 1965; Grigg and Alchin, 1976; Wood and Lenfant, 1976; Bartholomew, 1982). However, it also would be advantageous for lizards to attain their preferred body temperature as rapidly as possible after a dive in cold water. Water skinks may be more vulnerable to predator attack during the heating period because a lowered body temperature reduces the capacity for predator avoidance (Daniels, 1984). Clearly, evaporation either from the body surface or the respiratory tract has no significant effect on the rate of heating, particularly as dead lizards heated after a dive as rapidly as living ones (Daniels et al., in press). As with other reptiles (Voigt, 1975; Grigg and Alchin, 1976) it appears unlikely that the increased heart rates and breathing rates affect the rate of heating after emergence. More possibly, the elevated rates may be associated with the replenishment of oxygen stores, removal of any lactate from the tissues, and the repayment of the oxygen debt, incurred by diving. Reptiles frequently exhibit an increased heart rate after activity or diving (e.g. Licht, 1965; Huggins et al., 1969; Pough, 1973; Wood and Johansen, 1974; Heatwole, 1977; Butler and Jones, 1982; Seymour, 1982) and may also show an increased ventilation frequency (Butler and Jones, 1982). After a forced dive, breathing can begin immediately, with ventilation rates reaching ten times the pre-dive levels in turtles (Kooyman, 1973; Jackson and Silverblatt, 1974). In turtles high breathing

Diving adaptations of small lizards

rates, often associated with a decreased tidal volume, continue until blood gas tensions return to normal (Jackson and Silverblatt, 1974). However, some reptiles do not exhibit changes in ventilation frequency after activity but hyperventilate by increasing tidal volume (Bennett, 1973; Wood and Lenfant, 1976). Some diving reptiles have large tidal volumes (Seymour, 1982). Although tidal volumes were not quantified for either S. quoyii or C. robustus, qualitative observations suggest that it also increases after the dive. S. quoyii and C. robustus exhibited higher heart rates and breathing rates during heating than during cooling but cooled faster than they heated (Daniels et al., in press). Moreover, dead lizards heated and cooled at the same rate as living ones (Daniels, 1984; Daniels et af., in press). Such a response negates the hypothesis that increases in heart and breathing rates affect the thermoregulatory process. Heart rate may increase during heating to maintain blood pressure which presumably decreases in response to the peripheral vasodilation (White, 1976). Cooling may stimulate cutaneous vasoconstriction which may also reflexively 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 small lizards. CONCLUSION

Ctenotus robustus and adult and juvenile Sphenomorphus quoyii at 30°C possessed heart rates between

80 and 130 beats/min and ventilation frequencies between 32 and 42 breaths/min. All the lizards responded to submergence in cold water with a strong, instantaneous diving bradycardia similar to that observed for frightened reptiles. The strength of the diving bradycardia may be affected by both fear and water temperature. Stronger bradycardias occurred if submergence took place in water at a lower temperature than the pre-dive rr,. The strong diving bradycardia may decrease the rate of heat loss by severely reducing peripheral blood flow. Upon emergence, water skinks and robust skinks exhibited elevated heart rates and breathing rates while heating from 19.5 to 30°C compared to heating at rest. The increased heart and ventilation rates probably act to replenish depleted oxygen stores and remove lactate created in tissues respiring anaerobically during the dive. Lizards heated at the same rate after a dive and at a rest (Daniels et al., in press). If increased heart rates and ventilation frequency are indicators of physiological thermoregulation, then such responses are ineffective in comparison with environmental factors. At any T, both S. quoyii and C. robustus exhibited greater heart and breathing rates during heating at rest than during cooling. However, these lizards also cooled faster than they heated (Daniels et al., in press). Again increased heart and breathing rates during heating cannot be regarded as indicators of physiological thermoregulation. The responses to diving, heating after the dive and heating and cooling at rest were very similar for

197

robust skinks and water skinks, particularly when account was taken of the underlying interspecific and size differences. Thus it seems that S. quoyii does not possess any major thermoregulatory, ventilatory or cardiovascular adaptations to diving. Small skinks may be generally pre-adapted to diving, thus explaining why at least 20 species with a body mass less than 30 g regulatory utilize fresh or salt water for predator escape (Daniels, 1984). Acknowledgements-This study was supported by a Commonwealth Postgraduate Research Award to C.- B. D. J. Murray, M. P. Simbotwe, S. Phillips and G. Jenkins helped collect lizards. R. Hobbs and M. McCoy provided technical assistance, particularly with the computing, while V. Bofinger provided statistical advice. Sandra Higgins, Helen Jones and Julie Dodwell typed drafts of the manuscript.

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