Relationship Between Heart Rate and Oxygen Consumption During Steady-State Swimming in California Sea Lions

A number of workers have investigated the relationship between heart rate (fH) and rate of oxygen consumption ⁠, with a view to using the former to estimate the latter in free-ranging animals (see Butler, 1989, for a review). Certainly, under steady-state conditions, there is a good linear relationship between the two variables in most vertebrates that have been studied. Under natural conditions, however, animals may not always be in a steady state. Perhaps an extreme example of this is seen in aquatic birds and mammals during diving, when gas exchange is intermittent and there are large excursions in f_H associated with submergence and surfacing (Fedak et al. 1988; Butler, 1991, 1992). However, at the cellular level, these animals may be in a steady state (Butler, 1992). Despite the substantial variations in heart rate associated with diving activity, Fedak (1986) demonstrated that there was a linear relationship between fH and in a grey seal during increasing swimming activity if average and fH values over complete dive cycles were used. A similar situation has been described for two common seals and a sea lion (Williams et al. 1991).

The potential usefulness of/h as an indicator of aerobic metabolic rate in free-ranging marine mammals has been discussed by Butler (1992). A problem would be obtaining the data from animals at sea, and the only really feasible way of accomplishing this is to use data storage devices that can be retrieved from the animals at some stage. For Weddell seals, this has been achieved when they return to a breathing hole in the ice (Hill et al. 1987), but for most phocid seals recapture would only be reliably possible from one breeding season to the next. For otariids, however, the energetic cost of foraging could be determined using the heart rate method for breeding females, which return to their pups at regular intervals during the period of lactation (Gentry and Kooyman, 1986).

It was decided, therefore, to determine the relationship between fH and in the California sea lion, Zalophus californianus, at the temperature-controlled water channel facility, Scripps Institution of Oceanography, San Diego (see Feldkamp, 1987, for details).

Six subadult sea lions of either sex were used in the study. They had been beached and held for 1-3 months at Sea World, San Diego, before being transferred to the Physiological Laboratory at Scripps where they were kept in a circular channel for up to 30 days before being used. They were fed twice a day on a diet of herring and mackerel supplemented with vitamins. Their masses, just before the experiments, ranged from 25.7 to 38.1kg (mean 32.3±1.6kg S.E.).

The sea lions were trained to swim under a respirometer hood in the flume. As they could swim faster than the maximum water speed (1.4ms⁻¹) in the flume, the work load was increased by adding weights to a line and pulley attached to the back of the animal (see Williams et al. 1991, for details). When it was clear that each sea lion would swim for at least 15 min at 1.4 ms⁻¹, a data logger for capturing heart rate (Woakes, 1992) was placed within a sealed metal box attached to the back of the animal with epoxy glue. Two electrocardiogram (ECG) electrodes (self-adhesive human stress electrodes, NDM, Dayton Ohio) were placed on shaved, degreased skin in the mid line of the back at the levels of the pectoral and pelvic girdles, and attached to the data logger. These electrode positions gave clean ECG patterns, even in active animals. Plastic covers were placed over the electrodes and attached to the surrounding fur with epoxy glue. The animal was then placed into the test section of the water channel.

The animals were fasted for 18-24 h before an experiment and the water temperature was 22±1°C (range). Oxygen uptake was determined (see Davis et al. 1985; Feldkamp, 1987) while the animal rested or swam in the flume for 15 min at a controlled speed of up to 1.4 m s⁻¹ and pulling a weight of up to 3 kg. The combinations of water speed and load were chosen arbitrarily (see Woakes and Butler, 1983) but when resting values of the two variables were required the animals were left for more than one 15-min period before the next period of swimming. The data logger averaged and stored f_H every 30 s. Data were downloaded from the logger at the end of each experiment via a purpose-made interface to a lap-top computer (316LT, Dell). The mean values of f_H and of were taken over the last 5 min of each 15-min period, i.e. when had stabilized. Each animal was tested continuously for 24 h. Where appropriate, mean values are given±S.E. and all values of are at STPD. The Tukey multicomparison test was used to determine which regression slopes and then which elevations were significantly different from which others (Zar, 1984). Two lines were deemed to be significantly different from each other when α<0.05.

The lowest mean value of recorded from the six sea lions was 5.1±0.4mlmin⁻¹kg⁻¹ and the highest mean value (26.9±1.9mlmin⁻¹ kg’¹) was 5.3 times the resting value (Fig. 1). The lowest and highest values of/n were less extreme, the latter (155±5 beats min’¹) being only 2.2 times greater than the former (Fig. 1), which was 72±3 beats min⁻¹.

An example of the individual data points for a 24 h experiment with one sea lion is shown in Fig. 2 and this demonstrates the clear linear relationship between the two variables. All the individual linear regression lines, plus the mean of these, are illustrated in Fig. 3. The slopes (±s.E.) of the individual lines varied between 2.66±0.14 and 4.36±0.31 beats ml⁻¹ kg⁻¹, the intercepts varied between 48.2±3.5 and 63.0±2.3 beats min⁻¹ and r² varied between 0.82 and 0.93 (Table 1). The mean relationship for all six animals is fh = (57.4±2.0)+(3.58±0.23)⁠, r²=0.89±0.01. From Table 2 it can be seen that, for four pairs of regression lines, the slopes are significantly different from one another and for another five pairs, the elevations are significantly different.

The lowest mean value for is slightly less than the resting values reported by Feldkamp (1987) and Ponganis et al. (1991) (6.55 ml min⁻¹ kg⁻¹ and 6 ml min⁻¹ kg⁻¹, respectively) for California sea lions of a similar mass in the same swim flume. Although low water temperature is known to cause an increase in resting in this species, (T. M. Williams, R. W. Davis, S. Kanatous, A. J. Tirpak and I. L. Boyd, in preparation), water temperature cannot be the complete explanation for the difference between the present values and those values quoted above. The higher value obtained by Feldkamp (1987) was from animals in water at 27°C, while the animals used by Ponganis et al. (1991) were in water at 17°C. The lowest mean value obtained in the present study was only 20% greater than the standard metabolic rate for terrestrial mammals obtained from the allometric formula of Kleiber (1961), which is, (ml min⁻¹) = 10.13M⁰⁷⁵, where M is body mass in kg and assuming that 11 O₂=4.8kcal. These data support the proposal of Lavigne et al. (1986), that pinnipeds do not have a resting metabolic rate substantially above that of terrestrial mammals of similar body mass.

The highest mean obtained in the present study is similar to the values reported by Feldkamp (1987) and Williams et al. (1991) for sea lions swimming at an equivalent speed of approximately 3ms⁻¹, which is similar to the maximum surface swimming velocities measured in Galapagos and Hooker’s sea lions (Ponganis et al. 1990b). Also, Northern fur seals have mean swimming velocities of less than 2ms’¹ (Ponganis et al. 1992). None of the workers claim that their highest value is the maximum oxygen uptake for their animals. However, it is of interest that three of the same sea lions were used soon after the present study, and at the highest speed/mass load combination (1ms⁻¹, 4.5 kg) was approximately 30 ml min⁻¹ kg⁻¹ (T. M. Williams, R. W. Davis, S. Kanatous, A. J. Tirpak and I. Boyd, in preparation). In comparison, however, Ponganis et al. (1991) report a of 45 ml min⁻¹ kg⁻¹ in a California sea lion of 37 kg mass swimming at 1ms⁻¹ with a 4kg load. There is no obvious explanation for the difference in the recorded at similar work loads in these two studies, although the latter authors do state that their animals ‘only sustained this work load for short periods of time…. and obviously would not consistently work at this level’. It is not clear what Ponganis et al. (1991) meant by ‘short periods of time’, but wild terrestrial mammals will run for 5-15 min near or at (Taylor et al. 1981). We would suggest, therefore, that for the sea lions used in the above studies is somewhere between 30 and 40 ml min⁻¹ kg⁻¹, which is some 30-45% below the for a 32 kg wild terrestrial animal (Taylor et al. 1981). It is interesting to note that Costa et al. (1989), using the doubly-labelled water method, estimated the at-sea metabolic rate of foraging for 35 kg female Antarctic fur seals to be 29.3 ml min⁻¹ kg⁻¹. Also, Elsner (1986) reported a for 16–41kg harbor (common) seals of 33 ml min⁻¹ kg⁻¹ and the highest measured by Ponganis et al. (1990a) for 33 kg harbor (common) seals was 36 ml min⁻¹ kg⁻¹.

The important aspect, as far as the present study is concerned, is that the relationship was tested from resting to levels that are probably routinely reached in the wild. This indicates that f_H, recorded using data storage devices, could be used with otariids as an indicator of aerobic metabolism under field conditions and over extended periods (see Butler, 1992, for further discussion). From the present set of data, the mean formula for estimating from f_H is =(0.26±0.02)fh − (13.47±1.44), r²=0.89, where is in ml min⁻¹ kg⁻¹ and f_H is in beats min⁻¹. Clearly, it will be necessary to establish the details of the relationship between f_H and in other species but, if linearity is assumed, this could be achieved with two sets of data points (at rest and at a relatively high level of activity).

Experiments on aquatic and semi-aquatic birds have indicated that f_H is not a good predictor of for individuals, although it is very good if grouped data from a number of individuals are used (Bevan et al. 1992; Nolet et al. 1992). As 9 out of the 15 comparisons between pairs of linear regressions were significantly different in the present study, the need to use grouped data probably also applies to marine mammals. Bevan et al. (1992) have also demonstrated that this technique is accurate when the relationship between f_H and is derived from one group of birds and applied to another group of the same species. This is the case, even if the conditions under which the data were obtained are different e.g. at different environmental temperatures (Bevan and Butler, 1992). In this context, it appears that during swimming in California sea lions is independent of water temperature (T. M. Williams, R. W. Davis, S. Kanatous, A. J. Tirpak and I. Boyd, in preparation). Thus, it is concluded that the same constraints and advantages of the/H technique that have been described for aquatic birds exist for otariid seals.

This project is funded by NERC. The authors wish to thank Dr G. L. Kooyman, Dr T. M. Williams and Dr R. W. Davis and all those at the PRL, Scripps Institution of Oceanography, for their help and assistance. They also wish to thank Brad Andrews, Jim Antrim, Tom Goff and the animal care staff at Sea World for assisting in obtaining and holding the sea lions. This work was performed under permit no. 742 issued under the Marine Mammal Protection Act.