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Tift, MS, Huckstadt LA, Ponganis PJ.  2018.  Anterior vena caval oxygen profiles in a deep-diving California sea lion: arteriovenous shunts, a central venous oxygen store and oxygenation during lung collapse. Journal of Experimental Biology. 221   10.1242/jeb.163428   AbstractWebsite

Deep-diving California sea lions (Zalophus californianus) can maintain arterial hemoglobin saturation (S-O2) above 90% despite lung collapse (lack of gas exchange) and extremely low posterior vena caval S-O2 in the middle of the dive. We investigated anterior vena caval P-O2 and S-O2 during dives of an adult female sea lion to investigate two hypotheses: (1) posterior vena caval S-O2 is not representative of the entire venous oxygen store and (2) a well-oxygenated (arterialized) central venous oxygen reservoir might account for maintenance of arterial S-O2 during lung collapse. During deep dives, initial anterior vena caval S-O2 was elevated at 83.6 +/- 8.4% (n = 102), presumably owing to arteriovenous shunting. It remained high until the bottom phase of the dive and then decreased during ascent, whereas previously determined posterior vena caval S-O2 declined during descent and then often increased during ascent. These divergent patterns confirmed that posterior vena caval S-O2 was not representative of the entire venous oxygen store. Prior to and early during descent of deep dives, the high S-O2 values of both the anterior and posterior venae cavae may enhance arterialization of a central venous oxygen store. However, anterior vena caval S-O2 values at depths beyond lung collapse reached levels as low as 40%, making it unlikely that even a completely arterialized central venous oxygen store could account for maintenance of high arterial S-O2. These findings suggest that maintenance of high arterial S-O2 during deep dives is due to persistence of some gas exchange at depths beyond presumed lung collapse.

Ponganis, PJ, McDonald BI, Tift MS, Williams CL.  2017.  Heart rate regulation in diving sea lions: the vagus nerve rules. Journal of Experimental Biology. 220:1372-1381.   10.1242/jeb.146779   AbstractWebsite

Recent publications have emphasized the potential generation of morbid cardiac arrhythmias secondary to autonomic conflict in diving marine mammals. Such conflict, as typified by cardiovascular responses to cold water immersion in humans, has been proposed to result from exercise-related activation of cardiac sympathetic fibers to increase heart rate, combined with depth-related changes in parasympathetic tone to decrease heart rate. After reviewing the marine mammal literature and evaluating heart rate profiles of diving California sea lions (Zalophus californianus), we present an alternative interpretation of heart rate regulation that de-emphasizes the concept of autonomic conflict and the risk of morbid arrhythmias in marine mammals. We hypothesize that: (1) both the sympathetic cardiac accelerator fibers and the peripheral sympathetic vasomotor fibers are activated during dives even without exercise, and their activities are elevated at the lowest heart rates in a dive when vasoconstriction is maximal, (2) in diving animals, parasympathetic cardiac tone via the vagus nerve dominates over sympathetic cardiac tone during all phases of the dive, thus producing the bradycardia, (3) adjustment in vagal activity, which may be affected by many inputs, including exercise, is the primary regulator of heart rate and heart rate fluctuations during diving, and (4) heart beat fluctuations (benign arrhythmias) are common in marine mammals. Consistent with the literature and with these hypotheses, we believe that the generation of morbid arrhythmias because of exercise or stress during dives is unlikely in marine mammals.

McDonald, BI, Ponganis PJ.  2014.  Deep-diving sea lions exhibit extreme bradycardia in long-duration dives. Journal of Experimental Biology. 217:1525-1534.   10.1242/jeb.098558   AbstractWebsite

Heart rate and peripheral blood flow distribution are the primary determinants of the rate and pattern of oxygen store utilisation and ultimately breath-hold duration in marine endotherms. Despite this, little is known about how otariids (sea lions and fur seals) regulate heart rate (f(H)) while diving. We investigated dive f(H) in five adult female California sea lions (Zalophus californianus) during foraging trips by instrumenting them with digital electrocardiogram (ECG) loggers and time depth recorders. In all dives, dive f(H) (number of beats/duration; 50 +/- 9 beats min(-1)) decreased compared with surface rates (113 +/- 5 beats min(-1)), with all dives exhibiting an instantaneous f(H) below resting (<54 beats min(-1)) at some point during the dive. Both dive f(H) and minimum instantaneous f(H) significantly decreased with increasing dive duration. Typical instantaneous f(H) profiles of deep dives (>100 m) consisted of: (1) an initial rapid decline in f(H) resulting in the lowest instantaneous f(H) of the dive at the end of descent, often below 10 beats min-1 in dives longer than 6 min in duration; (2) a slight increase in f(H) to similar to 10-40 beats min(-1) during the bottom portion of the dive; and (3) a gradual increase in f(H) during ascent with a rapid increase prior to surfacing. Thus, f(H) regulation in deep-diving sea lions is not simply a progressive bradycardia. Extreme bradycardia and the presumed associated reductions in pulmonary and peripheral blood flow during late descent of deep dives should (a) contribute to preservation of the lung oxygen store, (b) increase dependence of muscle on the myoglobin-bound oxygen store, (c) conserve the blood oxygen store and (d) help limit the absorption of nitrogen at depth. This f(H) profile during deep dives of sea lions may be characteristic of deep-diving marine endotherms that dive on inspiration as similar f(H) profiles have been recently documented in the emperor penguin, another deep diver that dives on inspiration.

Williams, CL, Meir JU, Ponganis PJ.  2011.  What triggers the aerobic dive limit? Patterns of muscle oxygen depletion during dives of emperor penguins Journal of Experimental Biology. 214:1802-1812.   10.1242/jeb.052233   AbstractWebsite

The physiological basis of the aerobic dive limit (ADL), the dive duration associated with the onset of post-dive blood lactate elevation, is hypothesized to be depletion of the muscle oxygen (O(2)) store. A dual wavelength near-infrared spectrophotometer was developed and used to measure myoglobin (Mb) O(2) saturation levels in the locomotory muscle during dives of emperor penguins (Aptenodytes forsteri). Two distinct patterns of muscle O(2) depletion were observed. Type A dives had a monotonic decline, and, in dives near the ADL, the muscle O(2) store was almost completely depleted. This pattern of Mb desaturation was consistent with lack of muscle blood flow and supports the hypothesis that the onset of post-dive blood lactate accumulation is secondary to muscle O(2) depletion during dives. The mean type A Mb desaturation rate allowed for calculation of a mean muscle O(2) consumption of 12.4. ml O(2). kg(-1) muscle. min(-1), based on a Mb concentration of 6.4. g 100. g(-1) muscle. Type B desaturation patterns demonstrated a more gradual decline, often reaching a mid-dive plateau in Mb desaturation. This mid-dive plateau suggests maintenance of some muscle perfusion during these dives. At the end of type B dives, Mb desaturation rate increased and, in dives beyond the ADL, Mb saturation often reached near 0%. Thus, although different physiological strategies may be used during emperor penguin diving, both Mb desaturation patterns support the hypothesis that the onset of post-dive lactate accumulation is secondary to muscle O(2) store depletion.

Meir, JU, Ponganis PJ.  2010.  Blood temperature profiles of diving elephant seals. Physiological and Biochemical Zoology. 83:531-540.   10.1086/651070   AbstractWebsite

Hypothermia-induced reductions in metabolic rate have been proposed to suppress metabolism and prolong the duration of aerobic metabolism during dives of marine mammals and birds. To determine whether core hypothermia might contribute to the repetitive long-duration dives of the northern elephant seal Mirounga angustirostris, blood temperature profiles were obtained in translocated juvenile elephant seals equipped with a thermistor and backpack recorder. Representative temperature (the y-intercept of the mean temperature vs. dive duration relationship) was 37.2 degrees +/- 0.6 degrees C (n=3 seals) in the extradural vein, 38.1 degrees +/- 0.7 degrees C (n=4 seals) in the hepatic sinus, and 38.8 degrees +/- 16 degrees C (n=6 seals) in the aorta. Mean temperature was significantly though weakly negatively related to dive duration in all but one seal. Mean venous temperatures of all dives of individual seals ranged between 36 degrees and 38 degrees C, while mean arterial temperatures ranged between 35 degrees and 39 degrees C. Transient decreases in venous and arterial temperatures to as low as 30 degrees-33 degrees C occurred in some dives >30 min (0.1% of dives in the study). The lack of significant core hypothermia during routine dives (10-30 min) and only a weak negative correlation of mean temperature with dive duration do not support the hypothesis that a cold-induced Q(10) effect contributes to metabolic suppression of central tissues during dives. The wide range of arterial temperatures while diving and the transient declines in temperature during long dives suggest that alterations in blood flow patterns and peripheral heat loss contribute to thermoregulation during diving.

Meir, JU, Champagne CD, Costa DP, Williams CL, Ponganis PJ.  2009.  Extreme hypoxemic tolerance and blood oxygen depletion in diving elephant seals. American Journal of Physiology-Regulatory Integrative and Comparative Physiology. 297:R927-R939.   10.1152/ajpregu.00247.2009   AbstractWebsite

Meir JU, Champagne CD, Costa DP, Williams CL, Ponganis PJ. Extreme hypoxemic tolerance and blood oxygen depletion in diving elephant seals. Am J Physiol Regul Integr Comp Physiol 297: R927-R939, 2009. First published July 29, 2009; doi: 10.1152/ajpregu.00247.2009.-Species that maintain aerobic metabolism when the oxygen (O(2)) supply is limited represent ideal models to examine the mechanisms underlying tolerance to hypoxia. The repetitive, long dives of northern elephant seals (Mirounga angustirostris) have remained a physiological enigma as O(2) stores appear inadequate to maintain aerobic metabolism. We evaluated hypoxemic tolerance and blood O(2) depletion by 1) measuring arterial and venous O(2) partial pressure (PO(2)) during dives with a PO(2)/temperature recorder on elephant seals, 2) characterizing the O(2) hemoglobin (O(2)-Hb) dissociation curve of this species, 3) applying the dissociation curve to PO(2) profiles to obtain %Hb saturation (SO(2)), and 4) calculating blood O(2) store depletion during diving. Optimization of O(2) stores was achieved by high venous O(2) loading and almost complete depletion of blood O(2) stores during dives, with net O(2) content depletion values up to 91% (arterial) and 100% (venous). In routine dives (>10 min) Pv(O2) and Pa(O2) values reached 2-10 and 12-23 mmHg, respectively. This corresponds to SO(2) of 1-26% and O(2) contents of 0.3 (venous) and 2.7 ml O(2)/dl blood (arterial), demonstrating remarkable hypoxemic tolerance as PaO(2) is nearly equivalent to the arterial hypoxemic threshold of seals. The contribution of the blood O(2) store alone to metabolic rate was nearly equivalent to resting metabolic rate, and mean temperature remained near 37 degrees C. These data suggest that elephant seals routinely tolerate extreme hypoxemia during dives to completely utilize the blood O(2) store and maximize aerobic dive duration.

Ponganis, PJ, Kreutzer U, Stockard TK, Lin PC, Sailasuta N, Tran TK, Hurd R, Jue T.  2008.  Blood flow and metabolic regulation in seal muscle during apnea. Journal of Experimental Biology. 211:3323-3332.   10.1242/jeb.018887   AbstractWebsite

In order to examine myoglobin (Mb) function and metabolic responses of seal muscle during progressive ischemia and hypoxemia, Mb saturation and high-energy phosphate levels were monitored with NMR spectroscopy during sleep apnea in elephant seals (Mirounga angustirostris). Muscle blood flow (MBF) was measured with laser-Doppler flowmetry (LDF). During six, spontaneous, 8-12 min apneas of an unrestrained juvenile seal, apneic MBF decreased to 46 +/- 10% of the mean eupneic MBF. By the end of apnea, MBF reached 31 +/- 8% of the eupneic value. The t(1/2) for 90% decline in apneic MBF was 1.9 +/- 1.2 min. The initial post-apneic peak in MBF occurred within 0.20 +/- 0.04 min after the start of eupnea. NMR measurements revealed that Mb desaturated rapidly from its eupenic resting level to a lower steady state value within 4 min after the onset of apnea at rates between 1.7 +/- 1.0 and 3.8 +/- 1.5% min(-1), which corresponded to a muscle O(2) depletion rate of 1-2.3 ml O(2)kg(-1) min(-1). High-energy phosphate levels did not change with apnea. During the transition from apnea to eupnea, Mb resaturated to 95% of its resting level within the first minute. Despite the high Mb concentration in seal muscle, experiments detected Mb diffusing with a translational diffusion coefficient of 4.5 x 10(-7) cm(2) s(-1), consistent with the value observed in rat myocardium. Equipoise P(O2) analysis revealed that Mb is the predominant intracellular O(2) transporter in elephant seals during eupnea and apnea.

Meir, JU, Stockard TK, Williams CL, Ponganis KV, Ponganis PJ.  2008.  Heart rate regulation and extreme bradycardia in diving emperor penguins. Journal of Experimental Biology. 211:1169-1179.   10.1242/jeb.013235   AbstractWebsite

To investigate the diving heart rate (f(H)) response of the emperor penguin (Aptenodytes forsteri), the consummate avian diver, birds diving at an isolated dive hole in McMurdo Sound, Antarctica were outfitted with digital electrocardiogram recorders, two-axis accelerometers and time depth recorders ( TDRs). In contrast to any other freely diving bird, a true bradycardia (fH significantly < f(H) at rest) occurred during diving [dive fH (total beats/duration)= 57 +/- 2 beats min(-1), f(H) at rest= 73 +/- 2 beats min(-1) ( mean +/- s. e. m.)]. For dives less than the aerobic dive limit ( ADL; duration beyond which [ blood lactate] increases above resting levels), dive f(H)= 85 +/- 3 beats min(-1), whereas f H in dives greater than the ADL was significantly lower (41 +/- 1 beats min(-1)). In dives greater than the ADL, f(H) reached extremely low values: f H during the last 5 mins of an 18 min dive was 6 beats min(-1). Dive f H and minimum instantaneous f(H) during dives declined significantly with increasing dive duration. Dive f(H) was independent of swim stroke frequency. This suggests that progressive bradycardia and peripheral vasoconstriction ( including isolation of muscle) are primary determinants of blood oxygen depletion in diving emperor penguins. Maximum instantaneous surface interval f(H) in this study is the highest ever recorded for emperor penguins ( 256 beats min(-1)), equivalent to f(H) at V-O2 max., presumably facilitating oxygen loading and post-dive metabolism. The classic Scholander-Irving dive response in these emperor penguins contrasts with the absence of true bradycardia in diving ducks, cormorants, and other penguin species.

Ponganis, PJ, Stockard TK, Levenson DH, Berg L, Baranov EA.  2006.  Intravascular pressure profiles in elephant seals: Hypotheses on the caval sphincter, extradural vein and venous return to the heart. Comparative Biochemistry and Physiology a-Molecular & Integrative Physiology. 145:123-130.   10.1016/j.cbpa.2006.05.012   AbstractWebsite

In order to evaluate bemodynamics in the complex vascular system of phocid seals, intravascular pressure profiles were measured during periods of rest-associated apnea in young elephant seals (Mirounga angustirostris). There were no significant differences between apneic and eupneic mean arterial pressures. During apnea, venous pressure profiles (pulmonary artery, thoracic portion of the vena cava (thoracic vena cava), extradural vein, and hepatic sinus) demonstrated only minor, transient fluctuations. During eupnea, all venous pressure profiles were dominated by respiratory fluctuations. During inspiration, pressures in the thoracic vena cava and extradural vein decreased -9 to -21 mm Hg, and -9 to -17 mm Hg, respectively. In contrast, hepatic sinus pressure increased 2-6 mm Hg during inspiration. Nearly constant hepatic sinus and intrathoracic vascular pressure profiles during the breath-hold period are consistent with incomplete constriction of the caval sphincter during these rest-associated apneas. During eupnea, negative inspiratory intravascular pressures in the chest ("the respiratory pump") should augment venous return via both the venae cavae and the extradural. vein. It is hypothesized that, in addition to the venae cavae, the prominent para-caval venous system of phocid seals (i.e., the extradural vein) is necessary to allow adequate venous return for maintenance of high cardiac outputs and blood pressure during eupnea. (c) 2006 Elsevier Inc. All rights reserved.

Jobsis, PD, Ponganis PJ, Kooyman GL.  2001.  Effects of training on forced submersion responses in harbor seals. Journal of Experimental Biology. 204:3877-3885. AbstractWebsite

In several pinniped species, the heart rates observed during unrestrained dives are frequently higher than the severe bradycardias recorded during forced submersions. To examine other physiological components of the classic 'dive response' during such moderate bradycardias, a training protocol was developed to habituate harbor seals (Phoca vitulina) to short forced submersions. Significant changes were observed between physiological measurements made during naive and trained submersions (3-3.5min). Differences were found in measurements of heart rate during submersion (naive 18 +/-4.3 beats min(-1) versus trained 35 +/-3.4 beats min(-1)), muscle blood flow measured using laser-Doppler flowmetry (naive 1.8 +/-0.8 ml min(-1) 100 g(-1) versus trained 5.8 +/-3.9 ml min(-1) 100 g(-1)), change in venous P-O 2 (naive -0.44 +/-1.25 kPa versus trained -1.48 +/-0.76 kPa) and muscle deoxygenation rate (naive -0.67 +/-0.27 mvd s(-1) versus trained -0.51 +/-0.18 mvd s(-1), a relative measure of muscle oxygenation provided by the Vander Niroscope, where mvd are milli-vander units). In contrast to the naive situation, the post-submersion increase in plasma lactate levels was only rarely significant in trained seals. Resting eupneic (while breathing) heart rate and total oxygen consumption rates (measured in two seals) were not significantly different between the naive and trained states. This training protocol revealed that the higher heart rate and greater muscle blood flow in the trained seals were associated with a lower muscle deoxygenation rate, presumably secondary to greater extraction of blood O-2 during trained submersions. Supplementation of muscle oxygenation by blood O-2 delivery during diving would increase the rate of blood O-2 depletion but could prolong the duration of aerobic muscle metabolism during diving. This alteration of the dive response may increase the metabolic efficiency of diving.

Kooyman, GL, Ponganis PJ.  1994.  Emperor penguin oxygen consumption, heart rate and plasma lactate levels during graded swimming exercise. Journal of Experimental Biology. 195:199-209. AbstractWebsite

Oxygen consumption (V-O2), heart rate and blood chemistry were measured in four emperor penguins, Aptenodytes forsteri (Gray), during graded swimming exercise. The maximum V-O2, obtained, 52ml O-2 kg(-1) min(-1), was 7.8 times the measured resting V-O2 of 6.7 ml O-2 kg(-1) min(-1) and 9.1 times the predicted resting V-O2. As the swimming effort rose, a linear increase in surface and submerged heart rates (fH) occurred. The highest average maximum surface and submersion heart rates of any bird were 213 and 210 beats min(-1), respectively. No increase in plasma lactate concentrations occurred until V-O2 was greater than 25 ml O-2 kg(-1) min(-1). At the highest V-O2 values measured, plasma lactate concentration reached 9.4 mmol l(-1). In comparison with other animals of approximately the same mass, the aerobic capacity of the emperor penguin is less than those of the emu and dog but about the same as those of the seal, sea lion and domestic goat. For aquatic animals, a low aerobic capacity seems to be consistent with the needs of parsimonious oxygen utilization while breath-holding.