An analysis of electrocardiogram of alligator sinensis

Camp. Biochem. Physid. Printed in Great Britain

Vol.98A.

No. I. pp. 89-95. 1991 c

AN ANALYSIS OF ELECTROCARDIOGRAM ALLIGATOR SINENSIS

0300-9629/91 $3.00 + 0.00 1990 Pergamon Press plc

OF

WANG ZHAO-XIAN,*SUN NING-ZHEN, MAO WEI-PING, CHEN JIE-PING and HUANGGONG-QING~ Department of Biology, Nanjing Normal University, 122 Ninghai Road, Nanjing Jiangsu, PRC; tSuzhou Zoo, Suzhou, Jiangsu, PRC (Received 30 May 1990) Abstract-l.

ECG were recorded to determine the direction of atrial and ventricular depolarized waves and ventricular repolarized wave from Standard Limb Leads and Augmented Unipolar Limb Leads. 2. Statistical analysis was made, using six crocodiles at a measuring temperature of 22-25”C, on the time values and amplitudes of the waves from Standard Lead II as well as time duration of cardiac cycles concerning the initial heart rates, the R-T/R-R values and electrical axis of the QRS complex. The upward part of R waves generally displayed a variable notch. R wave’s time values and the direction of normal T wave differed from those reported concerning Alligator mississipiensis. 3. With extended voluntary apnoea, the amplitude and direction of P and T waves would change, resulting in an inverted P wave and an upright T wave. With R-R time extended, the values of R-T/R-R decreased substantially. 4. Along with the decrease of heart rates under voluntary dives, ECG T wave amplitude and direction changed, showing a relationship of T wave and breathing similar to that when the crocodiles were on

land.

INTRODUCTION

in the northern North Hemisphere, each on one side of the Pacific. It seems that there has been no studies reported concerning the ECG of the former species. This article specifically presents some electrocardiograms and analytical results on several of these crocodiles kept in a Zoo. The authors of this article observed the resulting ECGs and compared them with some available studies previously reported by others on Alligator mississipiensis and other species of crocodiles, and in addition, analysed the pulmonary breathing as well as the effects of diving activities on their ECGs.

The earliest documented electrocardiographic recordings of reptiles can be found in material presented by Buchanan (1909), who, using Einthovan’s methods and terminology, first reported three ECGs concerning a lizard, a snake and an Alligator mississipiensis. Later reports concerning the study of reptile ECGs tend to be of a simple descriptive nature, some without mentioning the animals’ body size or the temperatures under which the relevant ECGs were recorded, and very few, if any, mentioned the vector directions. There do exist some more detailed studies on Testudinata, Squamata, Ophidia and Tuatara rhynchocephaliu, reported by Kaplan and Schwartz (1963), Mullen (1967), Valantinuzzet et al. (1969a, 1969b) and McDonald and Heath (1971) respectively. However, documented ECGs of crocodiles can only be found in a few rather simple reports since Buchanan, i.e. Davies et al. (1951), concerning Crocodylus niloticus, Blackford (1956) and Wilber (1955, 1960), concerning Alligator mississipiensis. Andersen (1961), when studying Alligator mississipiensis’ diving physiology and biochemistry, made use of ECG recordings to measure the heart rates, incidentally mentioning the directional change of ECG T wave under submersion conditions, Huggins et al. (1969, 1970) observed, with ECG recordings, the variations of heart rates of Caiman sclerops and Alligator mississipiensis as well as the coupling re-

MATERIALS AND METHODS

The experiment took place in Suzhou Zoo, where the crocodiles studies were kept. A study on heart rates of Alligatorsinensis was reported in The breathing pattern and heart rates of Alligatorsinensis(Wang et al., 1990). In this article, we wish to concentrate on reporting the ECG recordings and analysing the statistical results. The data are essentially those measured in September 1986 under midautumn conditions with temperatures around 22-25°C. However, some of the experimental results obtained in October 1985 (early winter 17-19°C) are also included. For ECG recording methods as well as the methods and instrumentation for telemetric recording, see paper presented by Wang er al. (1990). ECGs were recorded from the standard bipolar limb leads I, II, and III, and also from augmented unipolar limb leads aVR, AVL and aVF.

sponses of breathing and heart rates of crocodiles. Alligator sinensis and Alligator mississipiensis are

RESULTS

two species in Subfamily Alligator, Order Crocodylia, Class Reptilia, which are the only existing crocodiles

*To whom all correspondence

Alligator sinensis’ Initial heart rates at the biginning of the recording period in a quiet state as well as the average ones over an extended period of time were reported in The breathing pattern and heart rates of Alligator sinensis (Wang et al., 1990).

should be addressed. 89

90

WANG

ZHAO-&AN

et a/,

the amplitudes and directions of P and T waves appeared to change with the variations in ventilation. tJ RS complexes

07 -....-A

J\

-

08 A

h

A

Q

I 0.5 mv 1 set

Fig. 1. ECG-tracings recorded with Standard Lead II on crocodiles Nos 09, 07 and OK

The ECGs recorded from ten crocodiles show no SV waves relating to the bioelectric activities of sinus vinosus of the hearts. Like the ECGs of other vertebrates, the strongest and most definite wave is the QRS complex of the ventricular depolarized process (Fig. 1). P wave and T wave, reflecting the atria1 depolarization and ventricular repolarization processes respectively, were recorded, but these waves were not constant. The cardiac cycles, heart rates and

ECGs were recorded from the Standard Leads, 1. Ii and III as well as the Augmented Unipolar Limb Leads. Typical tracings are shown in Fig. 2. The QRS complexes were R waves, a few crocodiles might show Rs waves from Lead II and II?, but no Q waves were observed. Statistical average amplitude of R waves for six crocodiles from Lead II was 0.21 mV (Table 1). The R wave voltage from Lead III was lower than that from Lead Il. The R wave voltage from Lead I was very low, and there were times when it was too low and flat to be recorded. The ventricular depolarization wave from the aVF Lead was identical to those from Leads II and III, and the voltage was somewhat lower than that from Lead II. The QRS complex waves from Lead aVR and aVL were QS waves. QRS complex durations of the ventricular depolarization in Altigaror sinensis we recorded are clearly longer than those of the mammals. The average R wave duration of six alligators was 0. I8 see {Table 2). The duration of R wave’s upward part was longer than that of the downward part. The wave forms of these animals’ R waves were often found to have a particular feature and were variable. Specifically. a notch was observed in the upward part of the R wave. i.e., the R wave rose slowly at first or had a plateau, followed by a steep elevation. R waves from Leads III and aVF were similar to those from Lead II. QS waves from Leads aVR and aVL displayed a downward curve at first, which might also have notches. From lead II, the specific part where the R wave notch appeared might vary. but never appeared in the

I

oVR 7r

v

Y

v

Y-

OVL

-

oVF

Fig. 2. ECG-tracings with Standard Leads 1, 11and 111as Nell as Augmented Unipolar Leads aVR, aVL and aVF on crocodile No. 04 at an ambient temperature of 18 C in October 1985.

KG

of Alligator sinensis

91

Table I. Amphtude and direction of ECG waves recorded with Standard Lead II, length of cardiac cycles and frontal plane of electric axis of QRS complex in AIIigaror sinensis at ambient temperature 22-25 C (Mean + SD) Amplitude Ammal NO.

Body wt. (kg)

Sex

8.5

01

F

OS

M

7,4

07

M

22.5

08

F

6.3

of ECG’ waves

--P WaYe (mv) 0.04 +- 0.01 fi2l -

R wave (mv)

T wave (mv)

R-R (set)

0.18 *0.01 (10) 0.16 + 0.01 (12) 0. I8 * 0.01 (12) 0.21 + 0.01

- 0.05 f 0.02 (10) - 0.06 & 0.02 (121 - 0.64 + 0.02 (12) - 0.05 * 0.01 (121 - 0.16 & 0.02 (14) - 0.03 * 0.00

2.22 I 0.04 (10) I .77 i: 0.03 (12) 2.44 2 0.66 (12) 1.95 i_ 0.02 (12) 2.27 i: 0.06 (14) 2.09 it 0.03

(12) 09 IO Overall The number

F

13.3

F

II.0

0.03 i 0.01 (14) -

average

0.40 + 0.01 (14) 0.15 i_ 0.02

(10)

(If.3

(10)

0.21 * 0.09

- 0.06 It 0.02

2.12 rt 0.24

of cardiac cycles used for statistics

Electric axis of R wave + 83 + 89 + 84 + 84 + 89 + 75 + 84. i: 5.1

are m parenthesis.

T waues

downward part. Moreover, the notch or plateau in the R wave might become so unclear that the R wave turned into a typical smooth line. The variable nature of the R wave’s upward part is yet to be clarified in terms of its patterns.

Like other reptiles, the T wave amplitudes and configurations of Alligator si~e~s~~ are prone to change. The authors of this article made synchronized recordings of the crocodiles breathing movements and ECGs, and the analysis of the results showed that pulmonary ventilation conditions were important factors determining the voltage and direction of ECG T waves. With more frequent ventilations and fast or medium heart rates, the T wave was always in the opposite direction compared with the main wave of the QRS complex (Table 2). On Leads II, III and aVF, T and R waves were in opposite directions, i.e. an inverted T wave (Fig. 1). Sometimes, T wave only represented a slight bend on the base line. On leads aVR and aVL, however, the QRS complex represented a QS wave under the base line, and the T wave was an upright one. But when the crocodiles were in quiet state with a prolonged apnoea or low breathing frequencies, the T wave voltage decreased, resulting in isoelectric potential,

The ampitude of P wave, which reflected the atrial depolarization, was very low. The P waves’ average duration in crocodile Nos 05 and 09 was 0.22 second (Table 2). When there was interference from muscle movements, the ECG base line showed some interfering vibration waves, affecting the identification of the low voltage P waves. Some ECGs never showed any P waves, even when the base line was stable. When the heart rates were slow owing to prolonged apnoea or low breathing frequency conditions, the P waves from Lead II. III and aVF were inverted, the durations were much shorter. and the voltage was very low, only showing some traces of depressions on the base line.

Table 2. Durations of EKG waves and ECG mtervals as well as the relatwe R-T values recorded wth Standard Lead II in .4/liga1or sinemiv at ambient temperature 22-25 C (Mean k SD) Durations of ECG’ wave and intervals

SW

Rody wt. (kg)

01

F

8.5

05

M

7.4

07

M

22.5

Ammalc NO.

08

F

P-R (SW)

021 0.02

(I3 -.

0 46 0.03 (121 -

6.3

R wave (secl

R-T (sect

0 14 0.02 110) 0.21 0.01 (12) 0.18 0.01 (12) 0.14 0.0 I

I .30 0.05 ilO)

(12) 09

F

13.3

IO

F

I I 0

Overall

The number

average

0 17 0.05 (14) .._

0.39 0.06 (I‘+) _.

0.19

0.43

0.24 0.00 (141 0 17 0.02 (11)) 0.18 0.04

of cardiac cycles used for statistics

I .08 0.05 03 I.48

0.03 (12) 1.30 0.05 (12) 1.35 0.04 (14) 1.29 0.04 .^ i1ut 1.30 0.13

are in pwenthesls.

R-R R-T;R-R (SEC) .._..-___ 0.32 0.02 (101 0.27 0.04 (12) 0.37 0.03 (12) 0.3 I 0.04 (121 0.42 0.04 (14) 0.25 0.03 .^ (II)) 0.32 0.06

7.22 0.04 (10) 1.77 0.03 (12) 2.44 0.66

0 59

0.68

0.61

(13 I .95

0.66

0.02 (I?) 2.27 0.06 (14) 2.09 0.03 00) 2.1 I 0.24

0.59

0.62

0.63

WANG ZHAO-XIAN et al.

92

Table 3. Variation of R-T intervals, relative R-T values and voltage as well as direction of ECG T waves in Alligaror sinensis Nos 09 and IO during the periods of faster and slower heart rates associated with frequent ventilation and extended aponea. Ambient temperature: 22-2x Animal NO.

Number of cardiac --cycles

09 09 09 09 10 10 IO 10

14 14 7

I IO Ii 9

1

R-R (see)

R-T (see)

2.27 2.73 1.21 14.08 2.09 4.01 9.23 14.30

1.35 I.59 2.00 2.20

--

1.29 I.81 2.33 2.40

R-T:R-R 0.59 0.58 0.27 0.16 0.62 0.45 0.25 0.15

T wave voltage (my) -.-.-.-0.16 - 0.08 + 0.05 + 0.05 - 0.03 - 0.03 + 0.06 + 0.08

thus the inversion of the direction. On Lead II, the original inverted T wave became an upright one and had a longer duration (Table 3). The authors succeeded in recording the dynamic process of the ECG T waves’ change along with that of pulmonary ventilations of crocodiles No. 03 and No. 09 (Fig, 3).

the time with which the excitation from atria traveled through the atrium-ventricle connection to the ventricular muscle. In the case of crocodile No. 09, the average value of the P-R interval duration at a heart rate of 26.5 beats/min was 0.39 sec. When the heart rate decreased to 22 beats/min, the P-R interval became 0.64sec. However, when the heart rate was reduced to a very low level, i.e. 8 beats/min, there was no further prolongation of the P-R interval. R-T intervals

This is the total time with which the depolarization and repolarization processes of the ventricular muscle was completed. The recording results showed that the Alligator sinensis’ R-T interval became longer with the slowing down of the heart rates, including the prolongation of the T waves. However, this prolongation applied mainly to the S-T segment from the end of R or Rs wave to the ~ginning of the T wave. The extent of R-T prolongation was far less than that of the slowing down of the heart rates.

ECG intervals

Statistical analysis was made concerning the crocodiles’ EGG P-R intervals, R-T intervals and the ratio of R-T/R-R under and ambient temperature range of 22-25’C (Table 3). P-R intervals

During the experiment, the P waves measured on most of the crocodiles’ Standard Leads and Augmented Unipolar Limb Leads ECGs were neither distinct nor constant. Crocodiles Nos 05 and 09 produced discernible P waves from some of the Lead II ECGs, allowing the measurement of P-R intervals, i.e. the depolarization process of the atria1 muscle and

values This is the ratio of ventricle muscle electric systole time and cardiac cycle time. Statistically, when the measured initial heart rates of the six crocodiles at an ambient temperature of 22-25°C were between 22-34 beats/min., the average value of R-T/R-R was 0.63 with the highest and the lowest being 0.58 and 0.68 respectively. For crocodiles Nos 09 and 10, when the instantaneous heart rates fell to 8 and 6.5 beats/min owing to prolonged apnoea, the values of R-T/R-R even fell to 0.16 and 0.15 for crocodiles Nos 09 and 10, when their longest cardiac cycles (14 set) were recorded (Table 3). R-T/R-R

10

s*c

Fig. 3. Representative records show the on-land respiratory-heart rate response and progressive changes of amplitude and direction of ECG T waves in crocodile No. 03 (upper graph recorded at ambient temperature 17-C) and No. 09 (lower graph recorded at 23’C).

ECG of Alligator sinensis

Electrical

axis of the heart

The instantaneous integrated QRS complex vector during the ventricle muscle depolarization process is called the QRS electric axis, which is often used in medicine to calculate the instantaneous integrated QRS electrical axis (frontal plane). The amplitude method for clinical measurement of human electrical axis of electrocardiogram involves calculation of QRS complex amplitude recorded with Lead I and Lead III as well as consultation of the relevant tables. Since Alligator sinensis’ ECG R wave recorded with Lead I had a very low voltage. The cardiac electrical axis was calculated from the amplitude of R waves recorded with Lead II and Lead III, using the measuring method on chickens as a reference. The crocodiles’ cardiac electrical axis of R wave (frontal plane) varied between + 75 and + 89 degrees at a temperature of 22-25°C (Table 1). Voluntary

diving-related

ECG variations

Heart rate slowing down was found by Wang et al. (1990) during the voluntary diving experiments on three crocodiles in a small pond in Suzhou Zoo. It came to the attention at the same time that the inverted T waves of crocodiles Nos 09 and 10 from Lead II ECG-tracings before submersion, which were in the opposite direction of the R waves, showed a gradual reduction in amplitudes during submersion and turned into upright T waves through an isoelectric potential stage (Fig. 4). DISCUSSION

Reptiles occupied a key position in the evolution of vertebrates. Researchers attach great importance to reptiles’ cardiac physiology, including the study of n

B

Fig. 4. ECG-tracing taken telemetrically during voluntary dives of a crocodile No. 09 show changes of heart rates and direction of ECG T waves. (A) Submerged in water pond, showing lengthened cardiac cacle length with upright T wave. (B) After the animal’s snout extended out of water to breathe air and resubmerged Smin, showing shortened cardiac cycle length with inverted T wave. (C) Resubmerged IOmin. (D) Resubmerged 40min. (E) 2 min after emergence.

93

their ECGs, mainly because of their characteristic heart structures and their blood circulation modes, which is the intermediate link in the evolution from fish’s single circulation to birds and mammals double circulation. Crocodiles heart structure is different from that of any other reptiles, with the two ventricular chambers completely separated. However, these ventricles are also different from those of birds and mammals, because crocodiles left and right aortic arches originate from right and left ventricles, respectively, i.e. the right aortic arch originates from the left ventricle, and the common pulmonary artery as well as the left aortic arch originate from the right ventricle. The bases of the left and the right aortic arches are connected by the foramen of Panizze. Contemporary researchers (White, 1970; Johansen, 1970; Tazawa and Johansen, 1986) suggested that during extended submersions, part of the crocodiles venous blood which has returned from systemic circulation back to the right ventricle can reenter that circulation directly through the left aortic arch without passing through pulmonary circulation. Conversely, during frequent breathing, the separation of systemic circulation blood and pulmonary circulation blood are quite complete, and the left and right aortic arteries are filled by oxygenated arterial blood which has gone through the pulmonary gas exchanges. Consequently, it is very meaningful to study crocodiles ECGs which have the above-mentioned heart structures and functional features. To interpret an animal’s ECG-tracings, one has to have an adequate knowledge of its cardiac histological structure, and especially, one has to make a comprehensive analysis of the morphological material concerning cardiac conduction system as well as the in vitro studying cardiac electro-physiological research data. Unfortunately, the existing anatomy data and results concerning crocodiles cardiac conduction system are to some extent confused or contradictory and there has been no report concerning in vitro studies on crocodiles cardiac electro-physiology. According to early documentations, there were different views among researchers as to the existence of a special excitation conduction system in crocodiles hearts. Nevertheless, the authors of this article are of the view that it is worthwhile to record and analyze ECG-tracings of Alligator sinensis, so that some possible features and patterns might be found. The heart position of Alligator sinensis, like the other reptiles-except some species of turtles such as Trionyx sinensis whose heart position is at the right side of the splanchnocoele central line-is on the vertical axis of the splanchnocoele central line, thus a very low voltage of the ECG waves from Lead I and the main wave of QRS complex from Leads II and III being also the R wave. However, the upward part of Alligator sinensis’ ECG R wave we recorded is usually characterized by variable notches. It is yet to be correctly determined whether this might be the result of time lag during the depolarization process of their right and left ventricle muscles owing to their particular heart structure and functioning or the result of the possible change in the excitation conduction of a specific part of the heart. Earlier ECG studies on Alligator mississipiensis and Crocodylus niloticus (Davies et al., 1951; Blackford, 1956; Wilber,

94

WANG ZHAO-XIAN et al

1955, 1960) were relatively brief, and did not mention the above features. It remains to be clarified whether this was because of the short recording times which failed to detect them or whether there exist no such features in the first place. According to Wilber (1960) the ECG-tracings’ R wave of 12 Alligator mississipiensis, 18-30 inches in length, recorded at 22°C had a time value of only 0.04 or 0.06sec (heart rate: 40 beats/min), while the time values of R wave we recorded on Alligator sinensis under 22-25°C being triple or quadruple of that. In addition, Blackford (1956) had reported in his study the ECG-tracing of a crocodile, Alligator mississipiensis recorded under anesthesia on a warm day in October at a heart rate of 50 beatsjmin, with the R wave lasting for 0.08 sec. Blackford did not give specification in terms of the body length and weight of the crocodile used in his measurement and the corresponding heart rates were higher than that we recorded on Alligator sinensis. Nevertheless. it seems quite surprising that there should be such a substantial difference between these crocodiles which both belong to Alligatoridae. Reptiles’ ECG-tracings are all characterized by the variability in their T wave amplitudes and vectors. Johansen (1959) had reported an increase in T wave amplitude when semiaquatic snake, Tropidonotus natrix was under forced submersion. Belkin (1964) had reported that inversion of the T wave of the turtles Pseudemys concinna was in association with breath. Wang and Liu (1986) had reported in their studies on Trionyx sinensis that, when the soft-shelled turtles were under faster heart rates conditions, the T wave on Lead I was an upright wave. With the development of bradycardia in forced submersion. the T wave voltage gradually decreased so low that it would become an inverted low-voltage T wave. (Further observations revealed that when the turtles showed a deepened asphyxia after several hours’ forced submersion, the T wave became upright again, with the amplitude elevated and the duration extended. The result of this observation not published). As far as crocodiles are concerned, it is yet to be determined whether the normal T wave is in the same direction or opposite direction compared with the R wave and whether it is an upright wave or an inverted wave. According to Davies et al. (1951). the T wave of Crocodylus niloticus was an inverted one. while according to Wilber (1955) the T wave of Alligator mississipiensis was an upright one, with the same direction as R wave. According to Andersen’s report (1961). prior to forced submersion, the Alligator mississipiensis had a normal upright ECG T wave from Lead II. During submersion and along with the reduction of the heart rates, the T wave became diphasic or even inverted direction and would return to upright wave when the heart rates increased after emergence. According to the ECG recordings we obtained with Alligator sinensis, it seems that when these animals were on land in an apparently quiet state with relatively high or medium heart rate. the T wave were usually inverted (during some cardiac cycles, the T waves diphasic merely representing a single baseline twist or with the same potential as the baseline). We believe. therefore, that the normal ECG T wave of the Alligator sinensis must be an inverted

one in the opposite direction of the R wave. It seems yet to be clarified why there is such a difference concerning Alligator sinensis’ ECG T wave direction and those of the Alligator mississipiensis in relevant reports. According to the results of simultaneous recordings of the Alligator sinensis’ on-land breathing actions and ECG-tracings, we are of the view that there must be a relationship between the T waves’ directional changes and the pulmonary ventilation and these changes are more or less progressive ones. When the crocodiles’ heart rates slowed down during voluntary diving which prevented them from pulmonary breathing, and when their heart rates accelerated after surfacing to breathe, the directional changes of the ECG T waves corresponded to the changes of the T waves with the ventilation status when they were on land. Furthermore, the inversion of the positive T waves might not necessarily be accompanied by the acceleration of the heart rates. and an indication of this assumption was observed in the following case: when crocodile No. 09 developed a bradycardia in a prolonged apnoea on land, hitting the tub in which it occupied only caused its ECG R-R’ length to change from 7.3 set (instantaneous heart rate 8.4 beats/min) to 6.2 set (instantaneous heart rate 9.6 beatsjmin). The ECG baseline showed some interfering waves but the upright T wave did not change direction. However, when the tub was hit again to give the crocodile some alarm excitation. the T wave was inverted, although R-R’s length was 5.2 set (instantaneous heart rate 11.5 beats/min) which did not represent an obvious acceleration of heart rates. From these results, we suggest that there might be a relationship between the change of T waves with the ventilation status and the respiratory gases content in the blood. The T wave amplitudes and directions in reptiles change with the ventilation status, it is quite an interesting and significant question whether there is a link between this phenomenon and the reported experimental ECG studies concerning the T wave changes resulting from changing the percentage contents of oxygen and carbon dioxide in inhaled air in dogs (Schafeer and Haas, 1962). The average R-T/R-R on Alligator sinensis’ initial heart rates ECG-tracings at 22-25-C is 0.63, which is close to what was reported concerning lizards and snakes (R-T/R-R: 0.61, Mullen, 1967) and Alligator mississipiensis (0.60. Wilber. 1955, 1960). Alligator sinensis’ R-T/R-R decreased from 0.63 at faster heart rates to below 0.27 or 0.25 at slower heart rates for crocodiles Nos 09 and 10 when they developed an extended apnoea or low breathing frequencies on land in a quiet state. This reflects an extension of total time of their ventricular depolarization and repolarization processes with the slowing down of the heart rates. However, this extension is not very long, suggesting that within a cardiac cycle, there are more times when not only the ventricle muscle has no mechanical movement, but also the bioelectric properties are in a static state. which naturally has its significances. According to the above observation and analysis, we believe that, in reptiles like Alligator sinensis, it might be appropriate to use their initial heart rates in experimentations as a reference to study their heart

EGG of Alligator sinensis

rate changes with behavior status and physiological actions under specific environmental and body temperature conditions. The heart rates slow down with the progress of extended non-ventilation (voluntary apnoea), and the T wave indicates a change in direction along with a substantial decrease in the value of R-T/R-R. As for the acceleration of heart rates in intensive movements, it can be considered as tachycardia. As soon as the crocodiles calm down, the heart rates returned to resemble the initial ones recorded at the beginning of the experiment. We discovered that the crocodiles’ heart rates could drop to a very low level when they developed bradycardia resulting from on-land long voluntary apnoea under a temperature of 22-25°C and the lowest level was very close to that of bradycardia caused by submersion or panic, and the T waves in both cases were also identical, This indicates a relationship between the terrestrial bradycardia-causing mechanism in voluntary apnoea and that of submersion. On the other hand, it is easy to understand the phenomenon in which the duration of low heart rates in submersion can be maintained longer than that of bradycardia in on-land long voluntary apnoea. since the crocodiles can effortlessly resume breathing from voluntary apnoea as long as they have the wish!

.4ckno~ledgemPnrs-The authors wish to express their gratitude to Professor Zhou Kai-Ya for his helpful comments and acknowledges Mr Yang Zuo-Xian for his technical assistance. This work was supported by a grant of Education Commission of Jiangsu Province, PRC.

95

Buchanan F. (1909) Note on the electrocardiogram, frequency of heartbeat and respiratory exchange in reptiles. J. Physiol. Proc. 39, xxv-xxvii. Davies F., Francis E. T. B. and King T. S. (1951). Electrocardiogram of the crocodilian heart. Nature 167, 146. Hugnins S. E.. Hoff H. E. and Pena R. V. (1969) Heart and respiratory rates in crocodilian reptiles under conditions of minimal stimulation. Physiol. Zool. 42, 32&333. Huggins S. E., Hoff H. E. and Pena R. V. (1970) The respiratory-heart rate response in crocodilian reptiles. Ph,vsiol. Zool. 43, 10-18.

Johansen K. (1959) Heart activity during experimental diving of snakes, Am. 1. PhysioE. 197, 604606. Johansen K., Lenfent C. and Hanson D. (1970) Phylogenetic development of pulmonary circulation Fed. Proc. 29, 1135-1140. Kaplan H. M. and Schwartz C. (1963) Electrocardiography in turtles. Life Sri. 2, 637-645. McDonald H. S. and Heath J. E. (1971) Electrocardiographic observation on the tuatara, Sphenodon punctatus. Comp. Biochem. Physiol. 4OA, 881-892. Mullen R. K. (1967) Comparative electrocardiography of the Squamata. Physioi. Zool. 40, 114126. Schafeer H. and Haas H. G. (1962) Electrocardiography. In handbook ofPhysio~ogy, Section 2, Circulation (Edited by Ham&on W. F. and Dow P.) Vol. I, pp. 323415. Am. Physiol. Sot., Washington, D.C. Tazawa H. and Johansen K. (1987) Comparative model analysis of central shunts in vertebrate cardiovascular systems Comp. Biochem. Physiol. 86A, 595607. Valantinuzzet M. E.. Hoff H. E. and Geddes L. A. (1969a) Observation on the electrical activity of the snake hear< J. Electrocardiol. 2, 39-50.

Valantinuzzet M. E., Hoff H. E. and Geddes L. A. (1969b) Electrocardiogram of the snake: effect of the location of the electrode and cardiac vectors. J. Electrocardiol. 2, 245-252.

Wang Z.-X. and Liu N.-S. (1986) Studies on the diving bradycardia of Trionyx sinensis. Acta Herpetologica Sinica 5, 17-23. REVERENCES

Andersen H. T. (1961) Physiological adjustments to crocodilian heart. Acra Physiol. &and. 53, 23-45. Belkin D. A. (1964) Variations in heart rate during voluntary diving in the turtle Pseudemys concinna. Copeia 1964, 321-330.

Blackford L. M. (I 956) The heart and electrocardiogram of an alligator. Circulation 14, 1114-l 116.

Wang Z.-X., Sun N.-Z., Mao W.-P., Chen J.-P. and Huang G.-Q. (1990) The breathing pattern and heart rates of AlBgator sinensis. Comp. Bibfhem. Physiol.

White F. N. (1970) Central vascular shunts in reptiles.’ Fed’Proc. 29, 1149-l 153. Wilber C. G. (1955) The electrocardiogram Biol. Bull. (Woods Hole) 109, 342. Wilber C. G. (1960) Cardiac responses of sipiensis to diving. Am. J. Physiol. 198,

and their control of the alligator. Alligator missis861-863.