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2018
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.

2017
Ponganis, PJ, McDonald BI, Tift MS, Gonzalez SC, DaValle B, Gliniecki RA, Stehman CC, Hauff N, Ruddick B, Howard R.  2017.  Effects of inhalational anesthesia on blood gases and pH in California sea lions. Marine Mammal Science. 33:726-737.   10.1111/mms.12388   AbstractWebsite

Despite the widespread use of inhalational anesthesia with spontaneous ventilation in many studies of otariid pinnipeds, the effects and risks of anesthetic-induced respiratory depression on blood gas and pH regulation are unknown in these animals. During such anesthesia in California sea lions (Zalophus californianus), blood gas and pH analyses of opportunistic blood samples revealed routine hypercarbia (highest P-CO2 = 128 mm Hg [17.1 kPa]), but adequate arterial oxygenation (P-O2 > 100 mm Hg [13.3 kPa] on 100% inspiratory oxygen). Respiratory acidosis (lowest pH = 7.05) was limited by the increased buffering capacity of sea lion blood. Amarkedly widened alveolar-to-arterial P-O2 difference was indicative of atelectasis and ventilation-perfusion mismatch in the lung secondary to hypoventilation during anesthesia. Despite the generally safe track record of this anesthetic regimen in the past, these findings demonstrate the value of high inspiratory O-2 concentrations and the necessity of constant vigilance and caution. In order to avoid hypoxemia, we emphasize the importance of late extubation or at least maintenance of mask ventilation on O-2 until anesthetic-induced respiratory depression is resolved. In this regard, whether for planned or emergency application, we also describe a simple, easily employed intubation technique with the Casper zalophoscope for sea lions.

Tift, MS, Huckstadt LA, McDonald BI, Thorson PH, Ponganis PJ.  2017.  Flipper stroke rate and venous oxygen levels in free-ranging California sea lions. Journal of Experimental Biology. 220:1533-1540.   10.1242/jeb.152314   AbstractWebsite

The depletion rate of the blood oxygen store, development of hypoxemia and dive capacity are dependent on the distribution and rate of blood oxygen delivery to tissues while diving. Although blood oxygen extraction by working muscle would increase the blood oxygen depletion rate in a swimming animal, there is little information on the relationship between muscle workload and blood oxygen depletion during dives. Therefore, we examined flipper stroke rate, a proxy of muscle workload, and posterior vena cava oxygen profiles in four adult female California sea lions (Zalophus californianus) during foraging trips at sea. Flipper stroke rate analysis revealed that sea lions minimized muscle metabolism with a stroke-glide strategy when diving, and exhibited prolonged glides during the descent of deeper dives (>100 m). During the descent phase of these deep dives, 55 +/- 21% of descent was spent gliding, with the longest glides lasting over 160 s and covering a vertical distance of 340 m. Animals also consistently glided to the surface from 15 to 25 m depth during these deeper dives. Venous hemoglobin saturation (SO2) profiles were highly variable throughout dives, with values occasionally increasing during shallow dives. The relationship between SO2 and flipper stroke rate was weak during deeper dives, while this relationship was stronger during shallow dives. We conclude that (1) the depletion of oxygen in the posterior vena cava in deep-diving sea lions is not dependent on stroke effort, and (2) stroke-glide patterns during dives contribute to a reduction of muscle metabolic rate.

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.

2014
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.

2013
McDonald, BI, Ponganis PJ.  2013.  Insights from venous oxygen profiles: oxygen utilization and management in diving California sea lions. Journal of Experimental Biology. 216:3332-3341.   10.1242/jeb.085985   AbstractWebsite

The management and depletion of O-2 stores underlie the aerobic dive capacities of marine mammals. The California sea lion (Zalophus californianus) presumably optimizes O-2 store management during all dives, but approaches its physiological limits during deep dives to greater than 300. m depth. Blood O-2 comprises the largest component of total body O-2 stores in adult sea lions. Therefore, we investigated venous blood O-2 depletion during dives of California sea lions during maternal foraging trips to sea by: (1) recording venous partial pressure of O-2 (PO2) profiles during dives, (2) characterizing the O-2-hemoglobin (Hb) dissociation curve of sea lion Hb and (3) converting the PO2 profiles into percent Hb saturation (SO2) profiles using the dissociation curve. The O-2-Hb dissociation curve was typical of other pinnipeds (P-50=28 +/- 2mmHg at pH 7.4). In 43% of dives, initial venous SO2 values were greater than 78% (estimated resting venous SO2), indicative of arterialization of venous blood. Blood O-2 was far from depleted during routine shallow dives, with minimum venous SO2 values routinely greater than 50%. However, in deep dives greater than 4. min in duration, venous SO2 reached minimum values below 5% prior to the end of the dive, but then increased during the last 30-60s of ascent. These deep dive profiles were consistent with transient venous blood O-2 depletion followed by partial restoration of venous O-2 through pulmonary gas exchange and peripheral blood flow during ascent. These differences in venous O-2 profiles between shallow and deep dives of sea lions reflect distinct strategies of O-2 store management and suggest that underlying cardiovascular responses will also differ.

2009
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.