The Transition Between Branchial Pumping and Ram Ventilation in Fishes: Energetic Consequences and Dependence on Water Oxygen Tension

Many species of fish are known to ventilate by keeping an open mouth when swimming, or by remaining stationary in a fast water current. Muir & Kendall (1968) termed this phenomenon ‘ram ventilation’. Ram ventilation has been repor-ted for mackerel (Scomber scomber, Hall, 1930), Remora remora (Strasbourg, 1957), sockeye salmon (Oncorhynchus nerka, Stevens & Randall, 1967; Smith, Brett & Davis, 1967) and a sharksucker (Echeneis naucrates, Steffensen & Lomholt, 1983).

The factors that regulate the transition from active to ram ventilation are not well understood (Ballintijn & Roberts, 1976; Roberts, 1978). Roberts (1974) reported ram ventilation in several species and presented evidence suggesting that the shift in mode of ventilation was independent of water oxygen tension and temperature. In a later study he concluded that the reflex transfer from active to ram ventilation is initiated by mechanoreceptors, and not by chemoreceptors (Roberts, 1975b).

The advantage of shifting the mode of ventilation is that this is likely to reduce the energetic cost of gill ventilation by transferring the work of breathing from the buccal and opercular pumps to the swimming muscles. Several approaches have been employed to estimate the cost of ventilation in resting fish and values from 0·5 to 45% of standard oxygen consumption have been reported (Van Dam, 1938; Schumann & Piiper, 1966; Alexander, 1967; Cameron & Cech, 1970; Davis & Randall, 1973; Jones & Schwartzfeld, 1974). Steffensen & Lomholt (1983) repor-ted an increase in standard oxygen consumption from 3·7 to 5·4% when the sharksucker shifted from ram to active ventilation. By contrast, there have been few studies of the cost of ventilation in swimming fish. Brown & Muir (1970) studied ram ventilation in skipjack tuna (Katsuwonus pelamis) and estimated the energetic cost of ventilation to lie between 1 and 3% of total metabolism. In swimming bass (Morone saxatilis) and bluefish (Pomatomus saltatrix) the cost was estimated to be 8·1 and 8·4%, respectively (Freadman, 1981).

The objectives of the present study have been to examine if the change in mode of ventilation in rainbow trout (Salmo gairdneri) and the sharksucker (Echeneis naucrates) depends exclusively on swimming speed or water velocity, or if it is also influenced by ambient water oxygen tension. If the latter is the case, both mechano-and chemoreceptors would be involved in eliciting the reflex transition in mode of ventilation. Furthermore, the energetic consequence of shifting to ram ventilation has been estimated for rainbow trout swimming at a constant speed.

Eight specimens of rainbow trout, Salmo gairdneri, were obtained from a local fish farm, and three specimens of the sharksucker, Echeneis naucrates, were collected in Florida and air freighted to Denmark. Total length and weight were A: 60cm, 820g, B: 63cm, 1275g and C: 65cm, 1500g. The sharksuckers were maintained at 23 °C and fed trout fillets ad libitum (Steffensen & Lomholt, 1983). The rainbow trout, weighing between 620 and 890 g, were kept in well-aerated large aquaria (10001) supplied with recirculating filtered water. The fish were fed trout pellets and the temperature was kept at 14-16°C.

Two types of experiments were done. First the water velocity at which the transition from active to ram ventilation takes place was determined by increasing the velocity in steps of 1 cms⁻¹ at different levels of water oxygen tension.

In the second series of experiments, the rate of oxygen consumption was compared for trout practising either active or ram ventilation while swimming at a constant speed. This was possible because, as shown below, trout swimming at a certain speed can be made to employ either active or ram ventilation by altering the water oxygen tension.

The experiments were conducted in a modified Brett-type swimming respiro-meter (Brett, 1964), with interchangeable swimming sections made from trans-parent PVC-tubing. For rainbow trout, a swimming section with an inner diameter of 15 cm was used and swimming speeds could be regulated up to 55 cm s⁻¹. When working on sharksuckers, a swimming section of inner diameter 12 cm provided with a convex surface at the top part was used, because the fish does not attach to a concave surface. In this case, water velocities up to 90cms⁻¹ could be obtained. Experimental temperatures were 15·0 ± 0·2°C for rainbow trout and 23·0 ± 0·2°C for sharksucker.

Mode of ventilation was determined by visual inspection of mouth and opercular movements. This way of monitoring the mode of ventilation may be criticized on the basis that very shallow ventilatory movements may not be detected. However, since the energetic cost of such possible undetected ventilatory movements must be very small, this will be of no consequence.

Swimming speeds at which the transition from active to ram ventilation takes place at different ambient oxygen tensions for eight rainbow trout are summarized in Table 1. At the lowest O₂ tension (50mmHg) some fish (II and IV) never showed steady ram ventilation even at the highest swimming speed of 55 cms⁻¹. In these cases there was no upper limit of the transition zone [indicated by ir, (irregular ventilation)]. Similarly, in hyperoxic water some individuals never showed regular active ventilation at the lower swimming speeds. Hence there was no lower limit to the transition zone, again indicated by ir in the table (fish I, III and IV).

The swimming speed required for transition from active to ram ventilation at different water oxygen tensions (⁠⁠) for trout VI is shown in Fig. 1. When swimming speed exceeds the lower limit of the transition zone, single breaths were dropped out. With increasing speed the drop-out sequences became longer, and when swimming speed rose beyond the upper limit of the transition zone, only ram ventilation was employed. In normoxic water this fish was ram ventilating at swimming speeds above 26cms⁻¹ In hypoxic water the threshold for ram ventilation was increased to a swimming speed of 43cms⁻¹, whereas in hyperoxia mmHg) it was decreased to 19cms⁻¹.

The asterisks in Fig. 1 indicate the combinations of swimming speed and oxygen tension at which oxygen consumption was measured. When swimming at 26 cms⁻¹ at 113–114 mmHg (*1) this trout ventilated actively and was 139·77 ± 4·70mgO₂kg⁻¹ h⁻¹. By increasing to 171–173 mmHg (*2) active ventilation was replaced by ram ventilation and decreased to 127·01 ± 3·75 mg O₂kg⁻¹ h⁻¹. The energy saving calculated as the percentage decrease in when shifting from active to ram ventilation was 9·1% (P> 0·005).

In order to determine whether this change in could be attributed solely to the cost of active ventilation and improved drag characteristics, or partly to a general increase in caused by an increased ventilatory requirement at the lower ⁠, oxygen consumption was measured at the same values as above, but at a swimming speed of only 10cms⁻¹ (asterisks 3 and 4). At this speed, the fish was only showing active ventilation, and was 90·66 ±5·38mgO₂kg ⁻¹ h ⁻¹ at 114-126 mmHg and 90·86 ± 9·92 mg O₂ kg⁻¹ h⁻¹ at 167-173 mmHg. A similar experiment was carried out on trout V. Student’s t-test showed no significant difference between these values. P. G. Bushnell (personal communication) likewise found identical oxygen uptake in trout swimming at 22 cms⁻¹ at of 60 mmHg and 120 mmHg, respectively. Consequently, the decrease in when swimming at 26-28 cms⁻¹ is an expression of the energy saved by the switch to ram ventilation.

Table 2 summarizes the experimental conditions and results of oxygen consump-tion measurements at different modes of ventilation. The calculated energy saving for fish V-VHI when swimming at 24-28cms⁻¹ varies from 8·4 to 13·3% of total oxygen consumption (mean ± S.D. = 10·2 ± 2·2%).

The velocity threshold required to elicit the transition to ram ventilation for three sharksuckers (Fig. 2) is clearly dependent on ambient oxygen tension in a manner similar to that seen in the trout (Fig. 1).

Correcting the water velocities is complicated when the solid blocking effect of the fish is high (Bell & Terhune, 1970). Hence in Fig. 2 uncorrected water velocities have been used. These will be lower than the velocities to which the fish have actually been exposed.

Since the water velocities in Fig. 2 are not corrected for the solid blocking effect of the fish, the velocities for the transition to ram ventilation in normoxic water read from Fig. 2 cannot be directly compared to the values in our previous study of the sharksucker (Steffensen & Lomholt, 1983), where the fish were so small that a correction was unnecessary. In fact the fish of the present study are the same animals which have, in the meantime, to some extent ‘outgrown’ the apparatus.

Rainbow trout reared on fish farms have been reported to have lost the ability to ram ventilate and will do so only after intensive training at high swimming speeds (Roberts, 1975a). Freadman (1979) reported that active ventilation was the only mode of ventilation used by rainbow trout up to a swimming speed of 70cms⁻¹, and he never observed the trout to ram ventilate. By contrast, the rainbow trout presently studied showed ram ventilation at swimming speeds as low as 20-30cms^−J in normoxic water (⁠ −150mmHg) without previous training.

The control of the transition between active and ram ventilation has been thought to be initiated largely through the action of mechanoreceptors detecting water pressure or velocity, whereas the transition is notably insensitive to water oxygen tension except at extreme, near lethal hypoxic conditions (Roberts, 1974, 1975a).

The present results are not in agreement with these earlier contentions. On the contrary, the swimming speed or water velocity necessary to elicit the transition from active to ram ventilation increases with declining ambient oxygen tension (Figs 1, 2, Table 1). This indicates that a stimulus is involved in controlling the ventilatory mode in rainbow trout and sharksucker, not only at extreme levels of oxygen tensions, but over the entire range of water oxygen tensions tested (approx. 75-300 mmHg).

Mackerel increase the gape in response both to an increased oxygen demand after feeding and to a lowered oxygen content of the water (Brown & Muir, 1970). A similar adjustment of mouth gape in response to water was observed during the present study in the swimming rainbow trout as well as in the resting sharksucker. This adjustment of mouth gape is clearly an indication that these fishes can also regulate gill irrigation in response to inspired during ram ventilation.

The energetic advantage of shifting the mode of ventilation is likely to be a result of a transfer of the work of breathing from the cranial respiratory muscles to the swimming musculature. Also ram ventilation may improve the drag characteristics of the swimming fish (Roberts, 1975a, 1978; Jones & Randall, 1978). During ram ventilation, the respiratory pump muscles are not relaxed, but tonically active and the mouth gape continuously adjusted, though the energetic cost of these move-ments is probably negligible (Freadman, 1979; Steffensen & Lomholt, 1983).

The observed decline in oxygen consumption is a measure of the total energy saving when shifting from active to ram ventilation. This saving was found to be from 8·4-13·3% of total oxygen consumption (mean di S.D. = 10·2 ± 2·2, Table 2). Since drag is most probably reduced because of improved boundary layer con-ditions resulting from a shift to ram ventilation (Roberts, 1975a, 1978; Freadman, 1979), a fraction of the 10·2% reduction can be ascribed to drag reduction. The exact magnitude of this fraction cannot be estimated at present. The remaining fraction of the average 10·2% reduction in can be ascribed to the cessation of activity of the branchial muscles. Consequently the oxygen consump-tion of the respiratory muscles must be somewhat less than 10% of total at a swimming speed just below the ram threshold. This low value is in good accord with the low cost of active ventilation seen in the sharksucker at rest which was 4-6% of standard oxygen consumption (Steffensen & Lomholt, 1983).

Ram ventilation is thus a mode of ventilation enabling the fish to save energy. This aspect of ram ventilation is particularly significant in the light of calculations by Jones (1971), which suggest that the oxygen consumption of the cardiac and branchial pumps may become so high as to limit maximal oxygen uptake.

The influence of ambient oxygen tension on the transition to ram ventilation as well as on the mouth gape during ram ventilation suggests that the control of this mode of ventilation forms an integral part of the control system of active branchial ventilation, which is primarily based on an oxygen-sensing mechanism (Dejours, 1975). The present study does not rule out the importance of mechanoreceptors for the initiation of ram ventilation, but indicates that these are strongly modulated by an oxygen-sensing mechanism.

I thank Professor K. Johansen and Dr J. P. Lomholt for valuable support and constructive criticism of the manuscript. This work was supported by a University of Aarhus research grant.