Camp. Biochem. Physiol. Vol. 89A, NO. 2, pp. 247-250, 1988 Printed in Great Britain

0300-9629/aa ~3.00 + 0.00 0 1988 Pergamon k~nals Ltd

BLOOD PRESSURES AND HEART RATES IN SWIMMING HAGFISH

M. E. FORSTER, P. S. DAVIE,* W. DAVISON, G. H. SATCHELL~ and R. M. G. WELLS$

Department of Zoology, University of Canterbury, Christchurch, New Zealand

(Received 13 May 1987)

Abstract-l. Ventral and dorsal aortic pressures and heart rates were measured in the New Zealand hagtish Eprntretus cirrhatus at rest, during forced exercise and on recovery from swimming.

4. Blood pressures were higher than those reported for the Atlantic hag&h, Myxine glutinosa, but were considerably lower than equivalent pressures found in teleost and elasmobranch fish.

3. The ventricular pressure pulse was always transmitted to the dorsal aorta and our evidence contradicts the view that branchial resistance is high in myxinoids.

4. Heart rates and ventral aortic pressures were higher after 10 min swimming, but the changes were not marked.

5. The tachycardia was continued into recovery. 6. The absence of bradycardia when the fish was disturbed (startle reflex) and the smooth increases

and falls in heart rates and pressures suggest that neural regulation of the heart is not important in swimming and that venous return may be the major factor determining cardiac function.

INTRODUCIION

In an unreported part of recent investigations of blood oxygen transport in free-swimming hagfish, Eptatretus cirrhatus (Wells et al., 1986), we measured blood pressures and heart rates using indwelling cannulae. In the branchial heart of hagfish the rate of rise of intraventricular pressure during systole is remarkably slower than in other vertebrates (Davie et al., 1987) and intravascular pressures are correspond- ingly low (Johansen, 1960; Jensen, 1965; Satchell, 1986). Indeed, it has been suggested that contrac- tion of the gill musculature during ventilation is important for the circulation of blood (Ho1 and Johansen, 1960).

Blood pressure measurements reported for the Atlantic hagfish, Myxine glutinosa, have been made on restrained animals. Work on this species is further hindered by its small size, being less than one tenth of the weight of the specimens of E. cirrhatus that we used. Our intravascular pressure measurements are the first to be made on unrestrained, free-swimming hagfish.

Another feature of interest of the hagfish heart is its apparent lack of vagal and sympathetic nervous regulation (Jensen, 1958). Hirsch et al., (1964) de- scribed nerve fibres and ganglion cells in the heart of E. stoutii, but Jensen (1965) suggested that the heart was functionally aneural. In support of this view, both Campbell (1970) and Laurent et al., (1982) note the comparative insensitivity of the myxinoid heart to exogenous cholinergic and adrenergic drugs. In tele- ost fish rapid modulation of cardiac function is possible through the action of the autonomic nervous system (Campbell, 1970; Laurent et al., 1982), and

Present addresses: *Department of Physiology and Anat- omy, Massey University, Palmerston North; tDepart- ment of Physiology, University of Otago, Dunedin and IDepartment of Zoology, University of Auckland, Auckland, New Zealand.

there is some evidence suggesting that catecholamines are involved in increasing the cardiac output in exercise (Randall, 1982).

The hagfish heart, in contrast, appears to change its rate and stroke volume as a direct response to an increase in its filling volume (Chapman et al., 1963; Satchell, 1986). We forced E. cirrhatus to swim to determine the response of the blood system to this physiological demand. An increased venous return, correlated with myotomal contractions, might then increase heart rate, allowing an increased cardiac output at a time of increased oxygen demand.

MATERIALS AND METHODS

Hagfish were collected off Motunau Beach, North Canterbury, New Zealand (43” 05’S, 173” 06’E) and for at least 1 week prior to use were held in running sea-water (16°C) in aquaria at the University of Canterbury. They were not fed. Nine animals were used in these experiments ranging in weight from 628 to 914 g.

Hagfish were anaesthetized in a solution of 0.04% benzo- caine.in sea-water. Under anaesthesia, a cannula was placed into the 6th or 7th left afferent branchial artery, with its tip l-2mm from the ventral aorta. A second cannula was placed into the dorsal aorta via a segmental artery craniad to the vent. Polyethlene cannulae (Portex) were used, with internal diameter greater than 1 mm, and they were filled with heparinized saline based on analysis of Myxine serum (Morris, 1965). Hagfish were allowed to recover from anaethesia and surgery for at least 16 hr prior to blood pressure measurements.

Blood pressures were measured using Bell & Howell pressure transducers (type 4-327) and were amplified and displayed on a Devices MX4 recorder. The traces were calibrated by recording the pressure of the sea-water surface and of columns of fresh-water above this surface. The hagflsh were forced to swim against a water current of 20 cmjsec, in an oval raceway previously described by Davie and Forster (1981). It was not necessary to use the electric grid at the downstream end, as the hagfish swam with little prompting. Heart rate readings, taken from the pressure records, are given at rest (before swimming commenced),

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248 M. E. FORS~ER et al.

60 s

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Fig. 1. Ventral and dorsal aortic pressures (in mm Hg) in a hagfish, 2Zptatreru.r cirrharus, at rest, during 12 min swimming and in recovery. Bottom two traces are a continuation of the top. The hagfish began

to swim at B and swimming ended at E.

after 10 min swimming and then at 1520 min post-swiming, the period labelled “recovery”.

Records were continuous, apart from the periods during which blood samples were taken for blood gas analysis. Mean blood pressures were calculated as l/3 systolic, 2/3 diastolic pressure. Results are given as means f standard error of the mean @EM). Student’s r-tests were used to establish the significance of paired differences.

RESULTS

We used wide-bore cannulae (2 mm i.d.) to connect the indwelling cannulae to the pressure transducers and these had to be long enough (c. 40 cm) to allow free movement of the animals. Despite the drag caused by the two cannulae, the hag&h were able to swim against a current of c. 0.35-0.4 body lengths/ sec. After 10 min swimming the hagfish showed signs of fatigue. Recovery blood lactate concentrations were still less than 0.5 mmol/l (Wells et al., 1986) but 15-20 min may not be a sufficiently long period to allow significant release of the anion from muscle.

Allowing for the extreme excursions of the pens caused by body flexions at commencement of swim- ming, there were no marked fluctuations of pressure at the onset of swimming and the heart rate was regular (Fig. 1). Heart rates increased on swimming and were 18% higher than resting values after 15 min recovery (Table 1.) Ventral aortic pressures rose by a small but significant amount on swimming, and then fell on recovery. There were no significant changes in dorsal aortic pressure (Table 1). Dorsal aortic pres- sure (8.0 mm Hg = 10.8 cm H,O = 1.07 kPa) was only 25% lower than ventral aortic pressure (10.8 mm Hg) at rest and 35% lower after 10 min swimming. Pulse pressures in the ventral aorta, at rest, ranged

from 2.2 to 4.5 mm Hg (mean 3.1 k 0.5 mm Hg). In the dorsal aorta the pulse pressure at rest averaged 0.9 + 0.7 mm Hg. Disturbances to the trace caused by swimming movements and a progressive attenuation for some records, which was probably due to partial occlusion of the cannulae, make other estimates of pulse pressure unreliable.

Resting ventilation rates were noted in three hagfish by observing the opening and closing of the branchial pores and the frequency (52-68 bpm) was found to be some 2-2.8 times higher than resting heart rates. Though coughs raised pressures in both ventral and dorsal aortas by 25% or more above normal systolic values (Fig. I), there was no evidence to suggest that movements of the ventilatory muscles were necessary for propulsion of blood to the post- branchial circulation. The pressure pulse associated with ventricular systole was always transmitted to the dorsal aorta (Fig. 1).

DISCUSSION

The dorsal aortic pressure in E. cirrharus is 54%

Table 1. Heart rates and blood pressures in swimming hagfish, Eptafre~us eirrhorus, at rest, after 10 min swimming and after 15 min

recowxv.

Heart rate (bpm) Ventral aorta P (mm Hg) Dorsal aorta P (mm Ha)

N Pre-swim Swimming Recovery

8 25.8 f 1.1 28.8 +_ 1.2’ 30.5 + 1.7**

6 10.8 f 0.7 11.6+0.5* 10.3 rtr 0.6

6 8.0 _+ 0.8 7.5 + 0.6 8.2 * 0.4

l Significantly different from pm-swimming values: *P < 0.05, l *P < 0.01.

Blood pressures in swimming hagfish 249

greater than that of anaesthetized M. glutinosa (Satchel], 1986). The actual difference, 2.8 mm Hg, is small and may reflect only the different conditions under which the measurements were made. The elec- trocardiographic and mechanical properties of the hearts of the two species are remarkably similar (Davie et al., 1987) and the slow rate of contraction of the ventricular muscle in myxinoids is suggested to be the main cause of the low systemic blood pressure. Dorsal aortic pressures in myxinoids are very much lower than those measured in teleost fish (Randall, 1970).

That resting mean dorsal aortic pressure is only 25% lower than mean ventral aortic pressure suggests that branchial resistance is not high in hagfish, de- spite claims to the contrary (Hardisty, 1979). Teleosts show a 40-50% drop in pressure across the branchial circulation and falls of 2540% are reported for elasmobranchs (Randall, 1970).

Our data show that contractions of the gill muscu- lature during ventilation do not play an essential role in the propulsion of blood into the dorsal aorta. In isolated, perfused rainbow trout gills Wood (1974) demonstrated that elevated efferent pressures de- creased branchial resistance. The abnormally low dorsal aortic pressures in Ho1 and Johansen’s (1960) experiments on Myxine may have resulted in such a high branchial resistance that transmission of ventric- ular systolic pressure to the dorsal aorta became impossible without the added force generated by coughs.

It is noteworthy that the heart of E. cirrhatus is able to increase its rate of beating during swimming and in recovery. On exercise, despite a relatively high oxygen affinity of its haemoglobin (P,, 12.3 mm Hg) there is significant desaturation of venous blood, with more than 80% of the oxygen being offloaded before blood returns to the heart (Wells et al., 1986). The heart lacks coronary arteries (Jensen, 1961; unpub- lished observations) and must depend upon venous blood for its own oxygen supply. A PVO* of 3-4 mmHg would seem to provide an extremely low driving force for oxygen delivery to the myocardial cells. Hansen and Side11 (1983) have demonstrated that the heart of Myxine can continue to function in anoxic conditions and after cyanide poisoning and our results suggest the heart of Eptatretus may also have good anaerobic capability. We noted no cardiac arrhythmias during swimming or recovery.

Without simultaneous measurements of cardiac output it is not possible to calculate changes in gill resistance. It is unlikely that significant changes in resistance occurred as there was a slight rise in ventral aortic pressure on swimming, associated with the elevated heart rate.

The fall in ventral aortic pressure on recovery, when heart rates had risen higher than when the hagfish was swimming, and at a time when dorsal aortic pressure is maintained, is consistent with a fall in branchial resistance. Elasmobranchs also failed to show marked changes in blood pressures on exercise (Johansen et al., 1966). By contrast, teleosts show large rises in ventral aortic pressure on swimming, with cardiac output increased and branchial vascular resistance reduced, particularly at fast speeds (Randall and Jones, 1978). Ideally, such comparisons

should be made with reference to maximal perfor- mance of the species being considered.

When the water current was increased sharply at the start of the exercise test there was no “startle reflex” (Fig. 1) (Stevens et al., 1972; Davie and Forster, 1980). Changes in heart rate and of blood pressure during swimming and recovery were slow and progressive. Taken together these two obser- vations are further evidence in support of the lack of neural regulation of the heart in myxinoids. The force of ventricular contraction has been shown to respond readily to end-diastolic volume (Chapman et af., 1963) and an augmented venous return may have been responsible for the increased ventral aortic pressure on swimming. The mechanisms re- sponsible for increased heart rates on swimming and in recovery await further investigation; with a poss- ible role here for subendocardial catecholamines (Helle et al., 1972).

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