Effects of training on forced submersion responses in harbor seals
Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093-0204, USA
*Present address: Loras College, 1450 Alta Vista, Dubuque, IA 52004-0178, USA (e-mail: pjobsis{at}uvi.edu)
Accepted August 16, 2001
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: dive response, heart rate, laser-Doppler, muscle blood flow, myoglobin, near-infrared spectroscopy, oxygen store, harbour seal, Phoca vitulina.
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
To examine physiological responses during submersions with heart rates greater than those observed during typical forced submersion studies, we attempted to habituate or train yearling harbor seals to short forced submersions, as has been done with ducks (Gabrielsen, 1985; Gabbott and Jones, 1987
). If a less intense bradycardia could be elicited during trained forced submersions, we wished to determine the effects of this on muscle blood flow, muscle oxygen depletion rates and post-submersion blood lactate levels. This is the first simultaneous measurement of these three variables in breath-holding animals.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Submersion training protocol
Once the seals had acclimated to the holding facilities, a submersion training protocol was begun. A submersion duration of 3 min was selected for seals lighter than 30 kg and 3.5 min for those above 30 kg. Both values are lower than the calculated aerobic dive limits for harbor seals and are within the common dive duration of free-diving harbor seals (Fedak et al., 1988; Kooyman, 1989
; Jobsis, 1998
). The training protocol consisted of conducting five forced submersions per day, each with a 20 min resting period, for approximately 10 (911) days over a 14-day period. The first session was always fully monitored (all recorded variables are described below), and all data collected during this first session were designated as naive. The last session was also fully monitored, and if the submersion heart rate (fH) response changed significantly, the data collected were designated as trained. In all intervening training sessions, only the electrocardiogram (ECG) and fH were recorded. Data obtained during naive and trained sessions were compared using a paired t-test (significance, P<0.05) and expressed as mean ± standard deviation (S.D.) unless noted otherwise. Following the fifth submersion of the trained session, one seal was subjected to a final 5 min submersion to detect changes in the submersion response when taken beyond the trained submersion duration.
At the start of each training session, a seal was weighed and restrained on a U-shaped restraining board. A clear Lucite diving helmet was placed over the head of the animal and loosely secured to the restraining board with elastic cord. The helmet used a two-layer neoprene gasket around the neck of the seal to prevent leaks. Room air was pumped through the helmet at 60 l min1. To avoid overheating, the seals were kept wet and cooled by air from an electric fan. To facilitate training, the durations of submersions and resting periods remained constant throughout all training sessions; visual and auditory cues were given to signal the beginning and end of each submersion, and all efforts were made to reduce or eliminate any discomfort experienced by the seals. To initiate a submersion, the draining valve of the helmet was closed (visual cue), the air pump was turned off (auditory cue) and fresh water, at ambient temperature, was poured into the helmet. When ending the submersion, the drain valve was opened and the air pump was turned on. The period from the initial visual cue to the start of submersion was approximately 15 s and that from opening the valve to the first breath at the end of submersion was approximately 10 s.
Oxygen consumption
In two seals, the rate of oxygen consumption was continuously monitored during naive and trained sessions by sampling the exhausted air from the helmet. The open-flow respirometry system was similar to the system described by Davis et al. (1985).
Heart rate
Three surface ECG electrodes were attached to each seal as described previously (Ponganis et al., 1997b). Recordings of ECG and fH were made during each submersion for all training sessions with a UFI (Morro Bay, California, USA) ECG/fH monitor and an Astro-Med eight-channel recorder. Heart rate was calculated as the total number of qrs waveforms in a given period divided by the duration of that period. Resting or pre-submersion heart rate was measured for a 1 min period 3 min before submersion. Heart rate during submersion is the mean rate during the entire submersion. The post-submersion period consisted of a 1 min period immediately following the end of the submersion period. After completion of the training protocol, the ECG electrodes were removed.
Anesthesia and blood sampling
All probe, catheter and electrode placements were conducted under local anesthesia (2 % Xylocaine and 0.25 % Bupivacaine) using aseptic techniques. All insertions were percutaneous, with a standard catheter-over-needle technique. For intramuscular probe insertions, the same technique was used with a peel-away catheter; this allowed removal of the catheter after insertion of the probe through it. At the time of catheterization, 1 g of cefazolin was given intravenously as an antibiotic prophylaxis. In addition, oral antibiotics, 1 g of cefalexin per day, were continued for 1 week following a monitored session. The insertion sites were monitored daily, and no seal showed any symptoms of infection following the procedure.
The extradural vein was catheterized at the start of naive and trained sessions using a 12.7 cm 14 gauge catheter. A heparinized saline (2 u.i. ml1 in 0.9 % NaCl) flush was used to maintain the catheter. Blood samples (3 ml) were taken 1 min before submersion (A), 30 s before the end of submersion (B) and 30 s (C), 2.5 min (D), 5 min (E) and 10 min (F) after the end of submersion. At 20 min after the end of submersion, the next pre-submersion sample (A) was taken. In seal W, sample B during the naive session was omitted. In seal S, the last in our protocol, an additional sample (1 ml) was taken 30 s after the start of submersion during the trained session. Sampling at this time may give a more accurate measure of pre-submersion venous oxygenation than sample A, which does not reveal the effects of pre-submersion hyperventilation by the seals. All blood samples were analyzed for PO2 with a Radiometer ABL2 blood gas analyzer. Plasma lactate and glucose concentrations were determined with a YSI lactate/glucose analyzer (YSI model 2300, Yellowsprings, Ohio, USA).
Muscle blood flow
Muscle blood flow was measured using two laser-Doppler blood flow (LDBF) meters. The first was a Transonics (Ithaca, New York, USA) ALF-21 LDBF monitor used for all four naive sessions and two trained sessions. Since this monitor was unavailable for two trained sessions, an Oxford Optronix (Oxford, UK) MPM 35 LDBF monitor was used. The catheter-like fiber-optic probe of the LDBF monitor was percutaneously placed into the ilioicostalis lumborum/longissimus dorsi (ILLD) muscle group 5 cm to the left of the spinal column, 2.5 cm above the crest of the ilium. Since two dissimilar LDBF meters were used and because the LDBF meters could not be calibrated in situ, muscle blood flow is given both as the absolute value provided by the factory calibrations and as a percentage of mean resting muscle blood flow (%RMBF), measured over 1 min, 3 min prior to each submersion. Muscle blood flow during submergence was measured by averaging over the entire submersion period. The post-submergence muscle blood flow was measured over the first minute following the submersion period.
Muscle oxygenation
Muscle oxygenation was monitored during naive and trained sessions by near-infrared spectroscopy (NIRS) (Jöbsis-VanderVliet et al., 1987). The Niroscope (Vander Corp., Durham, North Carolina, USA) uses NIRS to provide trend monitoring of combined oxyhemoglobin (HbO) and oxymyoglobin (MbO), combined deoxyhemoglobin (Hb) and deoxymyoglobin (Mb) and total hemoglobin (tHb). The data provided by the Niroscope show the change in the amount of HbO(+MbO), Hb(+Mb) and tHb in milli-vander units (mvd). The milli-vander unit is a measure of the relative change in the amount of HbO, Hb and tHb within the volume of tissue measured by the optical probes of the Niroscope. The standard surface probes of the instrument were replaced with a 17 gauge catheter-like fiber-optic probe with four emitter fibers at the tip and eight detector fibers recessed 0.5 cm from the tip (Jobsis, 1998
). The probe was percutaneously placed 5 cm to the right side of the spinal column and 2.5 cm above the crest of the ilium into the ILLD muscle group. The blunt tip of the probe was used to puncture the fascia of the muscle group and was inserted approximately 1 cm into the muscle. To reduce the possibility of interference between the Niroscope and LDBF light-emitting probes, the probes were placed on opposite sides of the spinal column.
Spontaneous apneas
During resting periods, the seals voluntarily performed spontaneous apneas, designated in this study as a voluntary apnea greater than 30 s. Heart rate, muscle blood flow and muscle oxygenation were recorded during spontaneous apneas and compared with those of naive and trained submersions as well as resting conditions. Blood sampling occasionally corresponded with these spontaneous apneas, but the sampling protocol was not altered. If a scheduled submersion occurred during a spontaneous apnea, the seal was awakened and allowed to resume a normal respiratory pattern before the scheduled submersion. Results are presented as means ± S.D. unless stated otherwise.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
O2 consumption
The mean oxygen consumption rate of two seals during a naive submersion session was 8.0±1.7 ml O2 min1 kg1. After training, the oxygen consumption rate of these two seals was 7.8±0.7 ml O2 min1 kg1 (N=2), which was not statistically significantly different.
Heart rate response
Heart rate during submersion showed a marked increase with training in three of the four seals (Fig. 1). In these three habituated seals, the mean fH during naive submersions, 18±4.3 beats min1, was significantly different from the mean fH during trained submersions, 35±3.4 beats min1 (Table 1). The onset as well as the overall fH of the submersion bradycardia showed differences between naive and trained submersions. During naive submersions, the drop in fH was nearly instantaneous, often with the lowest fH early in the submersion. During trained submersions, the fH decreased more gradually, and the lowest fH values were usually recorded at the end of the submersion. This is demonstrated by comparing the mean fH during the first 30 s of submersion. In naive submersions, the fH for this period was 18±4.8 beats min1, and in trained submersions the rate was 47±12.3 beats min1. The mean submersion fH increased steadily over the training period (Fig. 2), with the first submersion of each training session often having the lowest fH. The fH while resting prior to submersion and the tachycardia observed after submersion showed no statistical difference between naive and trained sessions, and fH was 111±22 beats min1 while resting and 154±6.1 beats min1 during the post-submersion tachycardia. Seal L, which did not significantly change its fH with training, had a submerged fH of 20±2.4 beats min1 during naive sessions and 21±2.7 beats min1 during trained sessions. This seal consistently showed the naive response in other variables as well.
|
|
|
In seal L, no significant differences were found between naive and trained submerged muscle blood flow; muscle blood flow was 1.2±0.5 ml min1 100 g1 (4.8±2.0 %RMBF) during naive submergence and 1.1±0.4 ml min1 100 g1 (6.5±2.4 %RMBF) during trained submergence. The post-submersion muscle blood flow values for this animal were unique in that they were lower than the resting level; 8.8±4.2 ml min1 100 g1 (35.5±16.9 %RMBF) during the first submersion session and 16.2±4.4 ml min1 100 g1 (95.3±25.9 %RMBF) during the last.
During the reduced muscle blood flow of naive submersions, small spikes in the muscle blood flow profile corresponded to individual heart beats. The muscle blood flow was low, continuous and variable during trained submersions and did not appear to be intermittently pulsatile (Fig. 3). In the rest period between submersions, muscle blood flow showed marked oscillations that corresponded to the breathing pattern of the animal. Perfusion increased during inspiration and decreased during expiration. The absence of this pattern was useful in identifying periods of spontaneous apnea.
|
|
Extradural vein PO2
Considerable variation was found when analyzing extradural vein samples taken during the naive and trained sessions for venous PO2 (PvO2). This variation appeared to be caused by the respiratory state of the animal since some samples were taken during spontaneous apneas while others were taken during the normal eupneic cycle. Indeed, the lowest PvO2 value (4.12 kPa) obtained occurred during a resting period while the seal was undergoing a spontaneous apnea and not during a submersion. As a result of this variation, the PvO2 values during naive and trained sessions at rest or at the end of submersion did not differ significantly. However, the difference in PvO2 between pre-submersion (sample A) and the sample taken during submersion (sample B) was significant. These decreases during submersion averaged 0.44±1.25 kPa for naive sessions and 1.48±0.76 kPa for trained sessions. This decrease in PvO2 may not represent the full drop in venous oxygen since sample A was taken before the pre-submersion hyperventilation and tachycardia. In one seal (seal S), a small sample was taken at the start of submersion during the trained session, and the PvO2 of these five samples was consistently higher than that of the A samples.
Plasma lactate levels
Plasma lactate concentrations increased and peaked early in the post-submersion period (Fig. 5). A significant increase in plasma lactate from the resting level to the post-submersion peak (2.5 min post-submersion) occurred during naive submersions for each seal except seal S. During trained submersion sessions, only seal W showed a significant increase in plasma lactate levels between resting levels and the post-submersion peak (30 s post-submersion). Although the concentrations were lower than those found in forced submersion studies with longer submersion durations (Scholander, 1940), the overall appearance of the lactate washout is similar.
|
The most consistent indicator of spontaneous apnea was a decrease in fH from the eupneic level of 110 beats min1 to the apneic level of less than 80 beats min1 (Fig. 3). For the three trained seals (W, A and S), the mean fH during spontaneous apnea was 60±7.5 beats min1 during naive sessions, which was significantly different from the value of 56±4.2 beats min1 occurring during trained sessions. In seal L, fH during spontaneous apneas of the naive session was 78±4 beats min1 and 66±6 beats min1 during spontaneous apneas of the trained session.
Muscle blood flow showed marked oscillations during the 20 min resting periods that reflected the pattern seen in the heart rate trace (Fig. 3) and corresponded to the breathing pattern. Spontaneous apneic muscle blood flow during naive and trained sessions of the three trained seals differed: during the naive sessions, it was 5.4±2.1 ml min1 100 g1 (30.9±14.1 %RMBF) and during the trained sessions it was 12.3±6.6 ml min1 100 g1 (46.6±26.7 %RMBF). For seal L, the spontaneous apneic muscle blood flows during naive and trained sessions were not significantly different. During both monitored sessions for all four seals, the spontaneous apneic muscle blood flow was always greater than muscle blood flow during submersion. Muscle deoxygenation rates during spontaneous apneas were lower in the trained sessions than in the naive sessions for the three trained seals. There was, however, considerable variation, and muscle oxygenation increased slightly during some spontaneous apneic events.
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Muscle blood flow
Muscle blood flow showed an obvious correlation with fH over the whole range of mean fH and muscle blood flow in this study (Fig. 6). Both linear and curvilinear regression analyses show a highly significant relationship (P<0.05). A second-order regression fitted the data best. This may be due to a difference between apneic and eupneic stroke volume (Ponganis et al., 1990) and to peripheral vascular regulation. However, the high degree of correlation may be misleading, for if one tests the relationship between fH and muscle blood flow taken during just one condition, such as post-submersion, there is a low degree of correlation and a significantly different regression line. This suggests that other factors, such as the intensity of local arterial constriction, may modify muscle blood flow during periods of similar heart rate.
|
The presence of a dense sympathetic innervation of proximal arterioles in pinnipeds (White et al., 1973) and the persistent muscle ischemia found in the presence of O2 depletion and lactate accumulation during forced submersions (Scholander, 1940
) suggest that regulation of muscle blood flow in seals is largely independent of local tissue metabolite control at the capillary level. Gooden and Elsner (1985
) have reviewed this concept of an extramuscular throttle for muscle blood flow. These authors also proposed that arteriolar smooth muscle perfusion and smooth muscle metabolite accumulation might be more critical regulators of arteriolar tone during intense sympathetic vasoconstriction. They hypothesized that local ischemia and metabolite accumulation in the more proximal vascular smooth muscle wall could result in an intermittent, pulsatile blood flow to the tissues even in the presence of continuous, intense sympathetic nerve activity. Such intermittent pulsations were not observed in this study, but have been reported in seal myocardial flow during forced submersions (Kjekshus et al., 1982
; Elsner et al., 1985
). Gooden and Elsner (1985
) also emphasized that a trickle of blood flow to the periphery could maintain perfusion of the arteriolar wall during severe (but incomplete) ischemia induced by sympathetic vasoconstriction. The muscle blood flow pattern, especially the persistent low degree of muscle blood flow found in naive seals with this protocol, is consistent with this latter mechanism. The even greater degree of muscle blood flow observed during trained submersions should not only be adequate for vascular smooth muscle perfusion, but should also be compatible with some degree of oxygen transport to skeletal muscle. Although the increased muscle blood flow during trained submersions appears to enhance the rate of blood oxygen depletion, this may actually maximize the duration of whole-body aerobic metabolism during diving, as suggested by Jobsis (1998
) and proposed in a theoretical model of O2 store utilization by Davis and Kanatous (1999
).
Remarkable regulation of muscle blood flow is depicted during the final 5 min submersion (Fig. 7) of seal S. This seal had been trained for 3 min submersions, but on the final submersion, the duration was extended to 5 min. During the first 3 min, fH and muscle blood flow were typical of the trained response. No cues were provided to the seal. However, at exactly 3 min of submersion, fH and muscle blood flow were lowered to levels found in the naive state and then maintained at that level until the end of the submersion. Such changes in peripheral flow probably also occur when fH changes abruptly during free dives (Andrews et al., 1997; Thompson and Fedak, 1993
). In this situation, blood O2 is maximally conserved for aerobic metabolism by the heart and central nervous system.
|
Spontaneous apnea
Spontaneous apnea provides an interesting comparison with the naive and trained submersions and provides a monitoring situation in which the apnea duration is under the control of the seal. Heart rate during spontaneous apneas was consistently higher than that found during trained submersions. The measured variables show a pattern that is consistent with an even greater peripheral perfusion during spontaneous apneas than during trained submersions. These measured variables include higher muscle blood flow and lower muscle oxygen depletion rates, suggesting a greater reliance on blood oxygen during spontaneous apneas than during trained submersions.
In conclusion, the training method used in this study was effective in habituating three out of four harbor seals to short forced submersions in which the heart rate response is more like that of free-diving harbor seals than that of typical forced submersion protocols. Although application of this technique is valuable because of the ability to make other physiological measurements, it must be remembered that it still differs from free diving by not mimicking the energy demands associated with swimming and foraging and by not duplicating the ability of the seal to determine submersion duration.
The seals that modified their responses showed significantly greater fH and muscle blood flow during trained versus naive submersions, but both variables were still reduced compared with the spontaneous apneic and eupneic levels. The increased muscle blood flow during submersion found in habituated seals was associated with a reduced rate of muscle deoxygenation and an increased rate of venous deoxygenation. In free-diving seals, such supplementation of the muscle oxygen store would delay the onset of anaerobic metabolism in the muscle and, thereby, decrease the metabolic cost of dives within the aerobic dive limit of the animal. These adaptations would potentially benefit the seals by increasing both the metabolic and foraging efficiencies during diving, as previously suggested by a mathematical model (Davis and Kanatous, 1999).
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Andrews, R. D., Jones D. R., Williams, J. D., Thorson, P. H., Oliver G. W., Costa, D. P. and Le Boeuf, B. J. (1997). Heart rates of northern elephant seals diving at sea and resting on the beach. J. Exp. Biol. 200, 20832095.
Blix, A. S., Elsner, R. W. and Kjekshus, J. K. (1983). Cardiac output and its distribution through capillaries and A-V shunts in diving seals. Acta Physiol. Scand. 118, 109116.[Medline]
Castellini, M. A., Milsom, W. K., Berger, R. J., Costa, D. P., Jones, D. R., Castellini, J. M., Rea, L. D., Bharma, S. and Harris, M. (1994). Patterns of respiration and heart rate during wakefulness and sleep in elephant seal pups. Am. J. Physiol. 266, R863R869.
Davis, R. W., Castellini, M. A., Kooyman, G. L. and Maue, R. (1983). GFR and hepatic blood flow during voluntary diving in Weddell seals. Am. J. Physiol. 245, R743R748.[Medline]
Davis, R. W. and Kanatous, S. B. (1999). Convective oxygen transport and tissue oxygen consumption in Weddell seals during aerobic dives. J. Exp. Biol. 202, 10911113.
Davis, R. W., Williams, T. M. and Kooyman, G. L. (1985). Swimming metabolism of yearling and adult Harbor seals (Phoca vitulina). Physiol. Zool. 58, 590596.
Elsner, R. W. (1965). Heart rate response in forced versus trained experimental dives in pinnipeds. Hvalråd. Skr. 48, 2429.
Elsner, R. W., Franklin, D., Van Citters, R. L. and Kenney, D. W. (1966). Cardiovascular defense against asphyxia. Science 153, 941949.[Medline]
Elsner, R. W., Millard, R. W., Kjekshus, J. K. and White, F. (1985). Coronary blood flow and myocardial segment dimensions during simulated dives in seals. Am. J. Physiol. 249, H1119H1126.[Medline]
Fedak, M. A. (1986). Diving and exercise in seals: interactions of behavior and physiology. In Behavioral Ecology of Underwater Organisms. Report of the 19th Symposium of the Underwater Association, March 2223, London. Prog. Underwater Sci. 11, 155169.
Fedak, M. A., Pullen, M. R. and Kanwisher, J. (1988). Circulatory responses of seals to periodic breathing: heart rate and breathing during exercise and diving in the laboratory and open sea. Can. J. Zool. 66, 5360.
Gabbott, G. R. J. and Jones, D. R. (1987). Habituation of the cardiac response to involuntary diving in diving and dabbling ducks. J. Exp. Biol. 131, 403415.[Abstract]
Gabrielsen, G. W. (1985). Free and forced diving in ducks: habituation of the initial dive response. Acta Physiol. Scand. 123, 6772.[Medline]
Gooden, B. A. and Elsner, R. W. (1985). What diving animals might tell us about blood flow regulation. Perspect. Biol. Med. 28, 465474.[Medline]
Grinnell, S. W., Scholander, P. F. and Irving, L. (1942). Experiments on the reaction between blood flow and heart rate in the diving seal. J. Cell. Comp. Physiol. 19, 341350.
Guppy, M., Hill, R. D., Schneider, R. C., Qvist, J., Liggins, G. C., Zapol, W. M. and Hochachka, P. W. (1986). Microcomputer-assisted metabolic studies of voluntary diving of Weddell seals. Am. J. Physiol. 250, R175R187.[Medline]
Guyton, G. P., Stanek, K. S., Schneider, R. C., Hochachka, P. W., Hurford, W. E., Zapol, D. G., Liggins, G. C. and Zapol, W. M. (1995). Myoglobin saturation in free-diving Weddell seals. J. Appl. Physiol. 70, 11481155.
Harrison, R. J. and Ridgway, S. H. (1975). Restrained and unrestrained diving in seals. Rapp. Pev. Réun. Cons. Int. Expl. Mer. 169, 7680.
Hill, R. D., Schneider, R. C., Liggins, G. C., Schuette, A. H., Elliott, R. L., Guppy, M., Hochachka, P. W., Qvist, J., Falke, K. J. and Zapol, W. M. (1987). Heart rate and body temperature during free diving of Weddell seals. Am. J. Physiol. 253, R344R351.
Hindell, M. A. and Lea, M. A. (1998). Heart rate, swimming speed and estimated oxygen consumption of free-ranging southern elephant seal. Physiol. Zool. 71, 7484.[Medline]
Jobsis, P. D. (1998). Muscle oxygenation and blood flow during submersion in ducks (Anas platyrhynchos) and seals (Phoca vitulina). PhD dissertation, University of California at San Diego. 142pp.
Jöbsis-VanderVliet, F. F., Fox, E. and Sugioka, K. (1987). Monitoring of cerebral oxygenation and cytochrome aa3 redox state. Int. Anesthesiol. Clin. 25, 209230.[Medline]
Kjekshus, J. K., Blix, A. S., Elsner, R., Hol, R. and Amundsen, E. (1982). Myocardial blood flow and metabolism in the diving seal. Am. J. Physiol. 242, R97R104.[Medline]
Kooyman, G. L. (1989). Diverse Divers. Berlin, New York, London: Springer-Verlag. 201pp.
Kooyman, G. L. and Campbell, W. B. (1973). Heart rate in freely diving Weddell seals (Leptonychotes weddellii). Comp. Biochem. Physiol. 43, 3136.
Murdaugh, H. V., Robin, E. D., Miller, J. E., Drewry, W. F. and Weiss, E. (1966). Adaptations to diving in the harbor seal: cardiac output during diving. Am. J. Physiol. 210, 176180.
Ponganis, P. J., Kooyman, G. L., Baranov, E. A., Thorson, P. H. and Stewart, B. S. (1997a). The aerobic submersion limit of Baikal seals. Can. J. Zool. 75, 13231327.
Ponganis, P. J., Kooyman, G. L., Castellini, M. A., Ponganis, E. P. and Ponganis, K. V. (1993). Muscle temperature and swim velocity profiles during diving in a Weddell seal (Leptonychotes weddellii). J. Exp. Biol. 183, 341346.
Ponganis, P. J., Kooyman, G. L., Winter, L. M. and Starke, L. N. (1997b). Heart rate and plasma lactate responses during submerged swimming and trained diving in California sea lions (Zalophus californianus). J. Comp. Physiol. B 167, 916.[Medline]
Ponganis, P. J., Kooyman, G. L., Zornow, M. H., Castellini, M. A. and Croll, D. A. (1990). Cardiac output and stroke volume in swimming harbor seals. J. Comp. Physiol. B 160, 473482.[Medline]
Ridgway, S. H., Harrison, R. J. and Joyce, P. L. (1975). Sleep and cardiac rhythm in gray seals. Science 187, 553555.[Medline]
Scholander, P. F. (1940). Experimental investigations on the respiratory function in diving mammals and birds. Hvalråd. Skr. 22, 1131.
Thompson, D. and Fedak, M. A. (1993). Cardiac responses of grey seals during diving at sea. J. Exp. Biol. 174, 139154.
White, F. N., Ikeda, M. and Elsner, R. W. (1973). Adrenergic innervation of large arteries in the seal. Comp. Gen. Pharmac. 4, 271276.
Williams, T. M., Kooyman, G. L. and Croll, D. A. (1991). The effect of submergence on heart rate and oxygen consumption of swimming seals and sea lions. J. Comp. Physiol. 160, 637644.
Zapol, W. M., Liggins, G. C., Schneider, R. C., Qvist, J., Snider, M. T., Creasy, R. K. and Hochachka, P. W. (1979). Regional blood flow during simulated diving in the conscious Weddell seal. J. Appl. Physiol. 47, 968973.