Metabolic Rates of Freely Diving Weddell Seals: Correlations With Oxygen Stores, Swim Velocity and Diving Duration

To construct reasonable models of the metabolism and the physiological constraints on the behavior of freely diving marine mammals, estimates of accessible body oxygen stores are divided by estimates of diving metabolic rate; the resulting time is defined as the approximate aerobic diving limit (ADL) and the results compared with dive duration/lactate appearance curves (Kooyman et al. 1980, 1983). The calculation of body oxygen stores available for diving involves summing the oxygen capacity of various tissues and estimating the level of oxygen extraction from these stores during the dive. While body oxygen stores are relatively straightforward estimates, determining to what level the oxygen stores are utilized during diving is complex and has only been achieved under artificial conditions of forced submersion in elephant seals (Elsner, 1969). It is even more difficult to estimate the metabolic rate in a freely diving seal and this value is usually extrapolated from exercise studies under non-field conditions or is taken from general relationships of mass vs metabolic rate.

Only one previous study has measured the oxygen consumption rates of seals diving under natural conditions. Kooyman et al. (1973) published oxygen consumption values for freely diving Weddell seals (Leptonychotes weddellii) in Antarctica. They built a large respirometry system over a hole in the sea-ice into which the seals could breathe after returning from dives. They concluded that diving was only about twice that at rest, much lower than the foraging metabolic rates estimated using different methods for fur seals and sea lions (Costa et al. 1989; Ponganis et al. 1990; Costa, 1991). However, because of the cumbersome methods used by Kooyman et al. (1973), the system could not be used to monitor the seals continuously over long periods or during periods of rapid change. Therefore, the range of behavior studied was limited.

The purpose of this project was to utilize modern methods of on-line computer-based monitoring to collect values of ⁠, continuously from Weddell seals during a range of activities and over long periods in order to test and to expand the earlier findings of Kooyman et al. (1973). Using the same basic animal handling methods of the earlier study, patterns of oxygen consumption were monitored during recovery periods from long and short dives, during bouts of sleep-associated apnea and during awake, rest periods.

Procedures for working with Weddell seals under free-diving conditions have been well documented and this study followed those general techniques (Kooyman, 1968; Kooyman et al. 1973). Five adult Weddell seals (average mass=355±59 kg; 3 females, 2 males) were captured on the sea-ice near McMurdo Station, Antarctica. The animals were weighed on a strain gauge cattle platform, accurate to ±1 kg, and then allowed to enter the sea water through a hole cut in the ice under a small portable heated laboratory.

Because the seals were confined to the study site, which was located several kilometers from any other breathing hole, they always came back to the ‘laboratory’. There were no other restrictions on the seals’ behavior and, over several days, they routinely made many short dives, some long dives, exhibited long bouts of sleep apnea, rested quietly and, in some cases, reamed at the hole to build an exit.

The methods used here were modeled on previous laboratory studies of computer-analyzed open-circuit oxygen consumption rates of seals in water (Davis et al. 1985; Fedak, 1986). Basically, once the animal was in the water, a large acrylic dome was placed over the hole and sealed against the water surface. Room air was moved through the dome at a rate of about 6001min^-1 using a vacuum motor. Exact flow rates for each experiment were determined by passing a known flow of 100 % nitrogen into the dome intake and measuring the change in oxygen content of the outflow air. A subsample of the outflow air was continuously drawn through water vapor and carbon dioxide extraction columns and then analyzed for oxygen content with an Ametek S3-A oxygen analyzer. The analog output of the oxygen analyzer was sent to a digital converter and then to an Apple computer. A BASIC program, modified from Davis et al. (1985) to provide more rapid sampling, collected the data and calculated the percentage of oxygen in the expired air and the oxygen consumption of the seal every 10 s. These data were reduced and analyzed using QUATTRO (Borland) and STATISTIX (Analytical Software) computer packages.

Resting oxygen consumption values were summed and averaged for seals that were quiet, awake and breathing regularly. For both dive and sleep apnea ‘events’, the oxygen consumption was summed for the time that the seal was breathing until the next event. During bouts of these activities, the recovery breathing period is short (less than 5 min; Castellini et al. 1988) and easily defined as the time until the next dive or breath-hold. For isolated dives interspersed with long periods at the surface, recovery was defined as the time at which oxygen consumption returned to resting values or when a period of sleep apnea began. The total amount of oxygen consumed during the recovery period was divided by the time of breath-holding plus the time of recovery. For example, for a 15 min dive with a 4min recovery, the oxygen used during the 4 min at the surface was divided by the total dive plus recovery time of 19 min to arrive at an oxygen consumption rate for the entire event. This oxygen consumption value was then plotted against the time of the breath-hold in order to relate oxygen consumption rates to dive or sleep apnea time.

On two of the five seals, swimming velocity was measured with a self-contained microprocessor-based paddlewheel assembly, as described in detail by Ponganis et al. (1990). The instrument was glued to the fur of the seals over the shoulder area. The microprocessor sampled swimming velocity every 7.5 s and logged the average velocity every 15 s. The minimum velocity that could be measured was 0.25ms^-1. When the experiment was finished, the instrument was removed from the seal and the data were transferred to a portable computer for analysis. Two additional animals were added to the study group for determination of swimming velocity only, providing a total of four seals in this section of the project.

During this study, 87 dives and 119 sleep apnea events were recorded for the five seals. Fig. 1 shows the frequency of dive and apnea events as a function of apnea time. Most dives (77 %) lasted less than 20 min with a modal diving time of 4.5 min and a maximum diving time of 82 min. All sleep-associated apnea events lasted less than 14 min (max=13.5 min) and had a modal time of 6 min.

The resting rate of oxygen consumption (RMR) for five seals was 4.1±0.3ml O₂min^-1 kg^-1 (±S.D.; Table 1) over a total recorded time of 8.8 h. In one seal that reamed at the ice hole, the metabolic rate was 5.6mlO₂min^-1kg^-1.

The metabolic rates for all dive ‘events’ (diving time plus recovery time) are averaged for each seal in Table 1. The individual rates of oxygen uptake for all 87 dives are plotted against diving time in Fig. 2. The average resting value of 4.1 ml O₂min^-1 kg^-1 is marked on the left-hand axis. There was a statistically significant decline in metabolic rate with diving time (unweighted least-squares linear regression test; P<0.005), but diving time accounted for only a small fraction of the variance (r²=0.27) in oxygen consumption (see Discussion). Because the theoretical ADL for adult Weddell seals of this mass is in the range of 14–15 min (Kooyman et al. 1980, 1983; Qvist et al. 1986), and because the maximum sleep apnea time was 13.5 min, the data were subsampled to include only those dive events that would be both clearly aerobic and comparable to sleep apnea durations. The average diving time of this ‘short dive’ (less than 14.0 min) subgroup was 5.5±3.1min (N=61) with an average oxygen consumption of 5.0±0.9 ml O₂min^-1 kg^-1. As with the preceding analysis, there was a significant negative correlation (P=0.009) between short diving times and metabolic rate, but high variance (r²=0.11). The average diving time of the ‘long dives’ (greater than 14.0min) was 31.0±14.1min with an average oxygen consumption of 3.4±0.6ml O₂ min^-1 kg^-1. As for short dives, there was a weak but significant decline in metabolic rate with longer diving time (r²=0.19; P=0.03).

For the 119 sleep apnea events monitored, the relationship of oxygen consumption to apnea time is shown in Fig. 3. Average metabolic rates during sleep for each seal are contained in Table 1. For this group of sleep apnea events, the average apnea time was 5.6±2.3min with an average oxygen consumption rate of 3.5±0.6ml O₂min^-1 kg^-1. There was a very weak relationship between oxygen consumption rate and sleep apnea duration (r²=0.05; P=0.01).

The mean oxygen consumption values (±standard deviation) for all conditions are given in Table 1. Kruskal-Wallis one-way nonparametric analysis of variance of resting, sleeping and all dive metabolic rates indicated that the three means were not different from one another (KW value=6.8; P=0.08). However, this comparison included the long dives that may have had a significant anaerobic component. Therefore, tests for differences in mean oxygen consumption rate were carried out on the same resting, sleeping and diving data set using only short dives and excluding those dives longer than 14min. When the long dives were excluded, the mean values for oxygen consumption during resting, sleeping and short diving were not equal (ANOVA nonparametric; P=0.03). To elucidate which of the means was different, a Tukey (HSD) pairwise comparison of means was conducted. This analysis indicated that the resting oxygen consumption value was not different from short diving or from sleeping values but that the sleeping and short-diving values were significantly different from one another. The oxygen consumption values for sleeping and short diving (Fig. 3) were further compared using a Student’ s t-test; this confirmed the Tukey analysis, indicating that the means were different (P<0.001). Therefore, it was concluded that oxygen consumption during short dives was not elevated over resting values but was statistically about 1.5 times elevated over sleeping apneas of similar duration.

8357 determinations of swimming velocity were made for four seals (Fig. 4). The modal velocity for three of the seals was about 2.0–2.1 m s^-1, while the fourth seal had a modal velocity of about 1.5 m s^-1. All the seals showed very little variation around the modal speed (72% of all velocities were within ±0.2ms^-1 of the mode).

The cost of diving in marine mammals is a difficult value to derive given the problems of assessing metabolic rate for an animal at sea. This problem has been approached in the past by extrapolating metabolic rate data from animals in swim flumes or small open-water pens (Ashwell-Erickson and Elsner, 1981; Davis et al. 1985; Fedak, 1986; Worthy et al. 1987; Feldkamp et al. 1989), but it is difficult in these approaches to model the free-ranging and varied behavior of unrestrained animals. Overall metabolic rates for free-ranging otariids have been estimated using the doubly labelled water technique (Costa and Gentry, 1986; Costa et al. 1989) but, although this technique is valuable for assessing energy balance equations, it is not detailed enough to separate the components of energy cost into periods of diving, sleep and rest. Generally, isotope turnover studies have estimated metabolic rate in otariids to be about 5–6 times higher than predicted standard metabolic rates (SMR) at swimming speeds that are equal to or less than those of Weddell seals (Costa and Gentry, 1986; Costa et al. 1989; Feldkamp et al. 1989; Ponganis et al. 1990). Thus, sea lions seem to swim more slowly than Weddell seals but to have a higher metabolic rate. Recent field metabolic rate studies of harbor seals also showed a metabolic rate about 5–6 times higher than predicted (Reilly and Fedak, 1991).

The average value for resting metabolic rate of the five seals in this study (4.1±0.3 ml O₂min^-1 kg^-1) was less than the value reported by Kooyman et al. (1973) for their five seals (5.1 ml O₂min^-1 kg^-1) despite the larger average size of the seals in the earlier study (425 kg vs 355 kg). Furthermore, the early study also included periods of sleep apnea in its average, which should have lowered the overall value for rest. The reason for the differences between the two studies is not known; however, both resting values exceeded the estimated metabolic rate for seals weighing about 350 kg based on the Kleiber ‘mouse to elephant curve’ (2.5 ml O₂ min^-1 kg^-1; Kleiber, 1961). This was probably because the basic requirements for measuring SMR could not be obtained in either study. That is, since these rest periods followed soon after dives that were probably for feeding, the seals were probably in a post-prandial state. If so, a food-induced thermogenesis component would have raised the metabolic rate. For example, sea otter RMR is over 50 % higher after they have eaten (Costa and Kooyman, 1984). Thus, the oxygen consumption values for both studies are higher than those that Lavigne et al. (1986a,b) have shown to occur under controlled laboratory conditions, where the metabolic rate of marine mammals can approach values of resting metabolic rate predicted from mass. However, the results of the current study tend to confirm the hypothesis of Bartholomew (1977) that ‘resting’ metabolic rates under field conditions are elevated and probably never reach predicted minimum values.

The relationship between the duration of all dives and oxygen consumption is statistically significant, but accounts for only 27 % of the variation in metabolic rate with dive duration. Much of the remaining variability is probably due to the behavioral requirements of short dives in which the cost of diving varies greatly (Fig. 2). In fact, when the short, aerobic dives are analyzed separately, the correlation between diving time and oxygen consumption is even weaker and dive duration accounts for only 10 % of the relationship. This is not surprising because short dives can involve hunting, local exploration and social or antagonistic activities involving differing levels of physical activity (Kooyman, 1968). The average value of oxygen consumption during these short dives (5.0±0.9ml O₂min^-1kg^-1) was not significantly different from oxygen consumption during rest (4.1±0.3mlO₂min^-1kg^-1). Kooyman et al. (1973) arrived at the same conclusion using different analytical techniques.

The rate of oxygen consumption during long dives (3.4±0.6mlO₂min^-1kg^-1) was also no different from the resting rate (t-test; P=0.06), but was significantly lower than the rate of oxygen consumption during short dives (t-test; P=0.01). However, because short dives are usually feeding dives (Kooyman, 1968), they may have an additional heat increment of feeding that would increase the metabolic rate. Also, the difference between long and short dives may be influenced by the fact that it can take a up to an hour for all the lactate produced during long dives to be processed (Kooyman et al. 1980). Thus, the actual oxygen consumption of long-term events may be spread over an extended recovery period or hidden in the cost of subsequent dives during which the lactate would continue to be processed (Castellini et al. 1988). In general, the recovery time between dives is short and constant in Weddell seals for dives below the ADL and increases rapidly for dives beyond the ADL (Kooyman et al. 1980; Castellini et al. 1988). Thus, the variation in metabolic rate for short dives is probably not closely related to patterns of surface recovery time.

The significant decline in metabolic rate with diving time indicates that diving metabolism is not constant in Weddell seals and tends to be lower with longer dives. It is intriguing, however, that the metabolic rate of the 82-min dive (3.0 ml O₂ min^-1 kg^-1) in seal no. 1 was within the standard deviation of the average metabolic rate for dives longer than 14min in this animal (seal no. 1, Table 1; Fig. 2; average metabolic rate for dives longer than 14 min and shorter than 82min is 2.6±0.6ml O₂min^-1 kg^-1). In other words, for dives beyond about 14min, in this seal, all the oxygen-conserving responses appear to have been invoked. It could also be that such fine detail of differences in oxygen consumption cannot be discerned by the methods utilized.

It is clear that diving, whether short or long, is not energetically costly in this species, and that the cost is much lower than the 4–6 times resting values measured in other diving species (Nagy et al. 1984; Costa et al. 1989; Davis et al. 1989; Costa, 1991; Kooyman et al. 1992; Reilly and Fedak, 1991).

The swimming velocities show that the seals swam at nearly constant speed. Thus, the histograms in Fig. 4 do not show a wide range of speeds but instead cluster about the mode. It is not known why three of the seals swam at about 2 ms^-1 and the fourth swam at about 1.5 ms^-1. Because no seals were monitored simultaneously for both velocity and oxygen consumption, direct correlations of these two data sets are not possible. However, the tight velocity distribution and the variable oxygen consumption pattern suggest that the two are not closely related in Weddell seals.

By dividing total body oxygen stores by the diving metabolic rate, a theoretical value for the aerobic diving limit can be derived. Available oxygen stores in the five seals were calculated to be 59mlO₂kg^-1 based on known relationships of respiratory and tissue oxygen capacities to body mass in Weddell seals (Appendix). Because the diving and resting metabolic rates were statistically similar, dividing the oxygen store by both metabolic rate values provides a range for the ADL from 9 to about 16 min (Table 2). Fig. 1 shows that most (70%) dives for Weddell seals in this study were within this calculated aerobic dive limit. By monitoring blood lactate values during free dives of various durations, Kooyman et al. (1980, 1983) have shown that the actual aerobic diving limit of adult and immature Weddell seals (140–450 kg) ranges from 10 to 19min. In the free-ranging situation, approximately 3–8% of all dives are beyond the calculated ADL (Kooyman et al. 1980,1983). However, because no blood lactate values were collected from the seals in this study, the theoretical ADL could not be verified.

Periodic breathing during periods of sleep in phocid seals is common (Bartholomew, 1954; Kooyman, 1968; Ridgway et al. 1975; Huntley, 1984; Castellini, 1991). In Weddell seals, it is known that long-duration sleep apnea appears to be aerobic with no significant build-up of lactate during or after the apnea (Kooyman et al. 1980). It is also known that several major physiological changes that occur during diving breath-holds also occur during sleep apnea: for example, significant and rapid cessation of ventilatory tachycardia and progressive hypoxia (for a review, see Castellini, 1991). The primary physiological differences between the two events are that the diving seal is exercising and its level of alertness is much greater. Thus, although both diving and sleeping conditions may have the same length of apnea, the sleeping seal is quiet while the diving seal is exercising. It is not surprising then that the metabolic rate during sleeping was less than that during diving events of the same duration. What is surprising is the relatively minor distinction: during diving was only 1.5 times that during sleeping. If it is assumed that the main difference between the two states is exercise, then some predictions can be made as to the cost of swimming, at the muscle level, in these seals.

Anatomical studies of phocids have shown that about 9–12 % of the body mass is propulsive muscle (Bryden and Felts, 1974; Fujise et al. 1985). Using this assumption, the average locomotory muscle mass of the Weddell seals in this study would maximally be about 42kg (0.12×355 kg). The difference in metabolic rate between the sleeping and diving seals is 1.5 ml O₂ min^-1 kg^-1 or 532 ml O₂ min^-1 for a 355 kg seal. Assuming that all of this difference is due to locomotory muscle activity, then an increase of 532 ml O₂ min^-1 during diving divided by 42 kg of muscle yields an addition in muscle metabolic rate over the sleeping rate due to exercise of about 12.7ml O₂ min^-1 kg^-1. Using estimates of resting muscle metabolic rates of about 1.5–2.0ml O₂min^-1 kg^-1 (Friedman and Selkurt, 1966; McGilvery, 1979), then exercising muscle would minimally consume about 14 ml O₂ min^-1 kg^-1 (12.7 ml O₂min^-1 kg^-1 + 1.5 mlO₂min^-1 kg^-1). Assuming that there is an oxygen store in the muscle of 60 ml kg^-1 [(45 g myoglobin kg^-1)×(1.34ml O₂g^-1 myoglobin); see Appendix], then the oxygen supply would last about 4–5 min [(60mlO₂kg^_1)/(14mlO₂min-¹kg-¹)] unless the circulation supplemented the oxygen stores or anaerobic muscle metabolism made a significant contribution during aerobic dives. Because anaerobic metabolism is not important during short dives (Kooyman et al. 1980, 1983; Guppy et al. 1986; Castellini et al. 1988), the circulation must either be open continuously or must pulse periodically to provide additional oxygen to the depleted tissue stores, as hypothesized by Kooyman (1987,1989) for skeletal muscle and Elsner et al. (1985) for cardiac muscle.

The relationship between dive duration and ADL in Weddell seals may not be directly applicable to other species of divers. Several species of otariids, and king and emperor penguins, appear to dive routinely beyond their theoretical ADL (Kooyman and Ponganis, 1990; Kooyman et al. 1992; Ponganis et al. 1992). In each of these cases, however, data on the diving metabolic rate or the blood chemistry necessary to confirm the ADL do not exist.

In conclusion, the data in this study show that there is a weak but significant inverse relationship in the Weddell seal between dive duration and metabolic rate, with the shortest dives having the highest metabolic cost. However, the cost of diving is not very great in freely diving Weddell seals and cannot be distinguished from resting values. Oxygen consumption during periods of sleep apnea is also no different from consumption at rest, but is about 1.5 times lower than exercise values. These low metabolic demands of diving help to explain the ability of this species both to dive for 15–20 min without shifting from aerobic-based metabolism and to dive for extremely long periods of up to 82 min.

Calculation of the available oxygen stores during diving are based on the following assumptions from Kooyman (1989): total blood volume is 14.8% of body mass, diving hematocrit is 58.0%, hemoglobin is 23.7 gm% and oxygen capacity is 32.5 vol%. Available blood oxygen is from arterial blood assumed to be 95% oxygen-saturated and extracted to 20% during the dive. Venous blood is 5vol% less than arterial blood and extracted to zero oxygen content. Venous fraction of total blood volume is 0.66. Myoglobin concentration is 45 gm kg^-1 muscle and myoglobin oxygen affinity is 1.34 ml O₂ g^-1 myoglobin. Muscle mass is 33% of total body mass. Diving lung volume is 50% of total lung capacity and oxygen concentration in the lung is assumed to be 15 %. Based on these values, the calculated total oxygen store available for an adult Weddell seal during a dive is about 59 ml O₂ kg^-1.

Field work was supported by NSF, Division of Polar Programs funding (NSF DPP 86-13729) to G.L.K. and additional analysis with NIH funding (R29 HL38765) to M.A.C. We would like to thank S. Eckert, E. Ponganis, K. Ponganis and P. Thorson for their help in instrument development and computer programming and for field assistance in the Antarctic.