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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.

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.

Tift, MS, Ponganis PJ, Crocker DE.  2014.  Elevated carboxyhemoglobin in a marine mammal, the northern elephant seal. Journal of Experimental Biology. 217:1752-1757.   10.1242/jeb.100677   AbstractWebsite

Low concentrations of endogenous carbon monoxide (CO), generated primarily through degradation of heme from hemeproteins, have been shown to maintain physiological function of organs and to exert cytoprotective effects. However, high concentrations of carboxyhemoglobin (COHb), formed by CO binding to hemoglobin, potentially prevent adequate O-2 delivery to tissues by lowering arterial O-2 content. Elevated heme-protein concentrations, as found in marine mammals, are likely associated with greater heme degradation, more endogenous CO production and, consequently, elevated COHb concentrations. Therefore, we measured COHb in elephant seals, a species with large blood volumes and elevated hemoglobin and myoglobin concentrations. The levels of COHb were positively related to the total hemoglobin concentration. The maximum COHb value was 10.4% of total hemoglobin concentration. The mean (+/- s.e.m.) value in adult seals was 8.7 +/- 0.3% (N=6), while juveniles and pups (with lower heme-protein contents) had lower mean COHb values of 7.6 +/- 0.2% and 7.1 +/- 0.3%, respectively (N=9 and N=9, respectively). Serial samples over several hours revealed little to no fluctuation in COHb values. This consistent elevation in COHb suggests that the magnitude and/ or rate of heme-protein turnover is much higher than in terrestrial mammals. The maximum COHb values from this study decrease total body O-2 stores by 7%, thereby reducing the calculated aerobic dive limit for this species. However, the constant presence of elevated CO in blood may also protect against potential ischemia-reperfusion injury associated with the extreme breath-holds of elephant seals. We suggest the elephant seal represents an ideal model for understanding the potential cytoprotective effects, mechanisms of action and evolutionary adaptation associated with chronically elevated concentrations of endogenously produced CO.

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.

2011
Sato, K, Shiomi K, Marshall G, Kooyman GL, Ponganis PJ.  2011.  Stroke rates and diving air volumes of emperor penguins: implications for dive performance. Journal of Experimental Biology. 214:2854-2863.   10.1242/jeb.055723   AbstractWebsite

Emperor penguins (Aptenodytes forsteri), both at sea and at an experimental dive hole, often have minimal surface periods even after performance of dives far beyond their measured 5.6 min aerobic dive limit (ADL: dive duration associated with the onset of post-dive blood lactate accumulation). Accelerometer-based data loggers were attached to emperor penguins diving in these two different situations to further evaluate the capacity of these birds to perform such dives without any apparent prolonged recovery periods. Minimum surface intervals for dives as long as 10 min were less than 1 min at both sites. Stroke rates for dives at sea were significantly greater than those for dives at the isolated dive hole. Calculated diving air volumes at sea were variable, increased with maximum depth of dive to a depth of 250 m, and decreased for deeper dives. It is hypothesized that lower air volumes for the deepest dives are the result of exhalation of air underwater. Mean maximal air volumes for deep dives at sea were approximately 83% greater than those during shallow (<50 m) dives. We conclude that (a) dives beyond the 5.6. min ADL do not always require prolongation of surface intervals in emperor penguins, (b) stroke rate at sea is greater than at the isolated dive hole and, therefore, a reduction in muscle stroke rate does not extend the duration of aerobic metabolism during dives at sea, and (c) a larger diving air volume facilitates performance of deep dives by increasing the total body O(2) store to 68 ml O(2) kg(-1). Although increased O(2) storage and cardiovascular adjustments presumably optimize aerobic metabolism during dives, enhanced anaerobic capacity and hypoxemic tolerance are also essential for longer dives. This was exemplified by a 27.6 min dive, after which the bird required 6 min before it stood up from a prone position, another 20 min before it began to walk, and 8.4 h before it dived again.

2010
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.

Shiomi, K, Narazaki T, Sato K, Shimatani K, Arai N, Ponganis PJ, Miyazaki N.  2010.  Data-processing artefacts in three-dimensional dive path reconstruction from geomagnetic and acceleration data. Aquatic Biology. 8:299-304.   10.3354/ab00239   AbstractWebsite

Tri-axis magnetism and acceleration data loggers have recently been used to obtain time-series headings and, consequently, the 3-dimensional dive paths of aquatic animals. However, problems may arise in the resulting calculation process with multiple parameters. In this study, the dive paths of loggerhead turtles and emperor penguins were reconstructed. For both species, apparently unrealistic movements were found. Time-series heading data of turtles showed small regular fluctuations synchronous with stroking. In the dive paths of penguins, infrequent abrupt changes in heading were observed during stroke cycles. These were unlikely to represent true behaviours according to observations of underwater behaviour and tri-axis magnetism and acceleration data. Based on the relationship between sampling frequency and frequency of body posture change, we suggest that (1) the changes in the animals' posture concurrent with strokes and (2) the mismatched treatment (i.e. filtering and non-filtering) of the acceleration and magnetism data caused the artefacts. These inferences are supported by the results of simulations. For data sets obtained at a given sampling frequency, the error pattern in calculated dive paths is likely to differ depending on the frequency and amplitude of body posture changes and in swim speed. In order to avoid misinterpretation, it is necessary to understand the assumptions and inherent problems of the calculation methods as well as the behavioural characteristics of the study animals.

Ponganis, PJ, Meir JU, Williams CL.  2010.  Oxygen store depletion and the aerobic dive limit in emperor penguins. Aquatic Biology. 8:237-245.   10.3354/ab00216   AbstractWebsite

The aerobic dive limit (ADL), dive duration associated with the onset of post-dive blood lactate elevation, has been widely used in the interpretation of diving physiology and diving behavior. However, its physiological basis is incompletely understood, and in most studies, ADLs are simply calculated with an O(2) store/O(2) consumption formula. To better understand the ADL, research has been conducted on emperor penguins diving at an isolated dive hole. This work has revealed that O(2) stores are greater than previously estimated, and that the rate of depletion of those O(2) stores appears to be regulated primarily through a diving bradycardia and the efficiency of swimming. Blood and respiratory O(2) stores are not depleted at the 5.6 min ADL determined by post-dive blood lactate measurements. It is hypothesized that muscle, isolated from the circulation during a dive, is the primary source of lactate accumulation. To predict this 5.6 min ADL for these shallow dives at the isolated dive hole with the classic O(2) store/O(2) consumption formula, an O(2) consumption rate of 2x the predicted metabolic rate of a penguin at rest is required. In contrast, if the formula is used to calculate an ADL that is defined as the time for all consumable O(2) stores to be depleted, then a 23.1 min dive, in which final venous partial pressure of oxygen (P(O2)) was 6 mm Hg (0.8 kPa), represents such a maximum limit and demonstrates that an O(2) consumption rate of about 0.5x the predicted rate of an emperor penguin at rest is required in the formula.

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.

Meir, JU, Ponganis PJ.  2009.  High-affinity hemoglobin and blood oxygen saturation in diving emperor penguins. Journal of Experimental Biology. 212:3330-3338.   10.1242/jeb.033761   AbstractWebsite

The emperor penguin (Aptenodytes forsteri) thrives in the Antarctic underwater environment, diving to depths greater than 500m and for durations longer than 23 min. To examine mechanisms underlying the exceptional diving ability of this species and further describe blood oxygen (O(2)) transport and depletion while diving, we characterized the O(2)-hemoglobin (Hb) dissociation curve of the emperor penguin in whole blood. This allowed us to (1) investigate the biochemical adaptation of Hb in this species, and (2) address blood O(2) depletion during diving, by applying the dissociation curve to previously collected partial pressure of O(2) (P(O2)) profiles to estimate in vivo Hb saturation (S(O2)) changes during dives. This investigation revealed enhanced Hb-O(2) affinity (P(50)=28mmHg, pH7.5) in the emperor penguin, similar to high-altitude birds and other penguin species. This allows for increased O(2) at low blood P(O2) levels during diving and more complete depletion of the respiratory O(2) store. S(O2) profiles during diving demonstrated that arterial S(O2) levels are maintained near 100% throughout much of the dive, not decreasing significantly until the final ascent phase. End-of-dive venous S(O2) values were widely distributed and optimization of the venous blood O(2) store resulted from arterialization and near complete depletion of venous blood O(2) during longer dives. The estimated contribution of the blood O(2) store to diving metabolic rate was low and highly variable. This pattern is due, in part, to the influx of O(2) from the lungs into the blood during diving, and variable rates of tissue O(2) uptake.

Ponganis, PJ, Stockard TK, Meir JU, Williams CL, Ponganis KV, Howard R.  2009.  O-2 store management in diving emperor penguins. Journal of Experimental Biology. 212:217-224.   10.1242/jeb.026096   AbstractWebsite

In order to further define O-2 store utilization during dives and understand the physiological basis of the aerobic dive limit (ADL, dive duration associated with the onset of post-dive blood lactate accumulation), emperor penguins (Aptenodytes forsteri) were equipped with either a blood partial pressure of oxygen (P-O2) recorder or a blood sampler while they were diving at an isolated dive hole in the sea ice of McMurdo Sound, Antarctica. Arterial P-O2 profiles (57 dives) revealed that (a) pre-dive P-O2 was greater than that at rest, (b) P-O2 transiently increased during descent and (c) post-dive P-O2 reached that at rest in 1.92 +/- 1.89 min (N=53). Venous P-O2 profiles (130 dives) revealed that (a) pre-dive venous P-O2 was greater than that at rest prior to 61% of dives, (b) in 90% of dives venous P-O2 transiently increased with a mean maximum P-O2 of 53 +/- 18 mmHg and a mean increase in P-O2 of 11 +/- 12 mmHg, (c) in 78% of dives, this peak venous P-O2 occurred within the first 3 min, and (d) post-dive venous P-O2 reached that at rest within 2.23 +/- 2.64 min (N=84). Arterial and venous P-O2 values in blood samples collected 1-3 min into dives were greater than or near to the respective values at rest. Blood lactate concentration was less than 2 mmol l(-1) as far as 10.5 min into dives, well beyond the known ADL of 5.6 min. Mean arterial and venous P-N2 of samples collected at 20-37 m depth were 2.5 times those at the surface, both being 2.1 +/- 0.7 atmospheres absolute (ATA; N=3 each), and were not significantly different. These findings are consistent with the maintenance of gas exchange during dives (elevated arterial and venous P-O2 and P-N2 during dives), muscle ischemia during dives (elevated venous P-O2, lack of lactate washout into blood during dives), and arterio-venous shunting of blood both during the surface period (venous P-O2 greater than that at rest) and during dives (arterialized venous P-O2 values during descent, equivalent arterial and venous P-N2 values during dives). These three physiological processes contribute to the transfer of the large respiratory O-2 store to the blood during the dive, isolation of muscle metabolism from the circulation during the dive, a decreased rate of blood O-2 depletion during dives, and optimized loading of O-2 stores both before and after dives. The lack of blood O-2 depletion and blood lactate elevation during dives beyond the ADL suggests that active locomotory muscle is the site of tissue lactate accumulation that results in post-dive blood lactate elevation in dives beyond the ADL.

2008
Shiomi, K, Sato K, Mitamura H, Arai N, Naito Y, Ponganis PJ.  2008.  Effect of ocean current on the dead-reckoning estimation of 3-D dive paths of emperor penguins. Aquatic Biology. 3:265-270.   10.3354/ab00087   AbstractWebsite

The dead-reckoning technique is a useful method for obtaining 3-D movement data of aquatic animals. However, such positional data include an accumulative error. Understanding the source of the error is important for proper data interpretation. In order to determine whether ocean currents affect dive paths calculated by dead-reckoning, as has previously been hypothesized, we examined the directions of the estimated positions relative to the known real points (error direction) and the relationship between the error direction and the current direction. 3-D dive paths of emperor penguins Aptenodytes forsteri diving at isolated dive holes in eastern McMurdo Sound were reconstructed by dead-reckoning, and the net error and error direction were calculated. The net error correlated positively with the dive duration. The error directions were not distributed uniformly, and the mean error direction tended to be north of the starting point of dives. Because there was a southward-flowing current in eastern McMurdo Sound, the ocean current was likely to affect the calculated dive paths. Therefore, the method of error correction generally used, in which the net error divided by the dive duration is applied to each estimated position, is realistically appropriate, provided that the current does not change significantly during a dive.

2007
Ponganis, PJ, Stockard TK, Meir JU, Williams CL, Ponganis KV, Van Dam RP, Howard R.  2007.  Returning on empty: extreme blood O-2 depletion underlies dive capacity of emperor penguins. Journal of Experimental Biology. 210:4279-4285.   10.1242/jeb.011221   AbstractWebsite

Blood gas analyses from emperor penguins (Aptenodytes forsteri) at rest, and intravascular P-O2 profiles from free-diving birds were obtained in order to examine hypoxemic tolerance and utilization of the blood O-2 store during dives. Analysis of blood samples from penguins at rest revealed arterial P(O2)s and O-2 contents of 68 +/- 7 mmHg (1 mmHg= 133.3 Pa) and 22.5 +/- 1.3 ml O-2 dl(-1) (N= 3) and venous values of 41 +/- 10 mmHg and 17.4 +/- 2.9 ml O-2 dl(-1) (N= 9). Corresponding arterial and venous Hb saturations for a hemoglobin (Hb) concentration of 18 g dl(-1) were > 91% and 70%, respectively. Analysis of P-O2 profiles obtained from birds equipped with intravascular P-O2 electrodes and backpack recorders during dives revealed that (1) the decline of the final blood P-O2 of a dive in relation to dive duration was variable, (2) final venous P-O2 values spanned a 40-mmHg range at the previously measured aerobic dive limit (ADL; dive duration associated with onset of post-dive blood lactate accumulation), (3) final arterial, venous and previously measured air sac P-O2 values were indistinguishable in longer dives, and (4) final venous P-O2 values of longer dives were as low as 1-6 mmHg during dives. Although blood O-2 is not depleted at the ADL, nearly complete depletion of the blood O-2 store occurs in longer dives. This extreme hypoxemic tolerance, which would be catastrophic in many birds and mammals, necessitates biochemical and molecular adaptations, including a shift in the O-2-Hb dissociation curve of the emperor penguin in comparison to those of most birds. A relatively higher-affinity Hb is consistent with blood P-O2 values and O-2 contents of penguins at rest.

Stockard, TK, Levenson DH, Berg L, Fransioli JR, Baranov EA, Ponganis PJ.  2007.  Blood oxygen depletion during rest-associated apneas of northern elephant seals (Mirounga angustirostris). Journal of Experimental Biology. 210:2607-2617.   10.1242/jeb.008078   AbstractWebsite

Blood gases (P-O2, P-CO2, pH), oxygen content, hematocrit and hemoglobin concentration were measured during rest-associated apneas of nine juvenile northern elephant seals. In conjunction with blood volume determinations, these data were used to determine total blood oxygen stores, the rate and magnitude of blood O-2 depletion, the contribution of the blood O-2 store to apneic metabolic rate, and the egree of hypoxemia that occurs during these breath-holds. Mean body mass was 66 +/- 9.7 kg (+/- s.d.); blood volume was 196 +/- 20 ml kg(-1); and hemoglobin concentration was 23.5 +/- 1.5 g dl(-1). Rest apneas ranged in duration from 3.1 to 10.9 min. Arterial P-O2 declined exponentially during apnea, ranging between a maximum of 108 mmHg and a minimum of 18 mmHg after a 9.1 min breath-hold. Venous P-O2 values were indistinguishable from arterial values after the first minute of apnea; the lowest venous P-O2 recorded was 15 mmHg after a 7.8 min apnea. O-2 contents were also similar between the arterial and venous systems, declining linearly at rates of 2.3 and 2.0 ml O-2 dl(-1) min (-1), respectively, from mean initial values of 27.2 and 26.0 ml O-2 dl(-1). These blood O-2 depletion rates are approximately twice the reported values during forced submersion and are consistent with maintenance of previously measured high cardiac outputs during rest-associated breath-holds. During a typical 7-min apnea, seals consumed, on average, 56% of the initial blood O-2 store of 52 ml O-2 kg(-1); this contributed 4.2 ml O-2 kg(-1) min(-1) to total body metabolic rate during the breath-hold. Extreme hypoxemic tolerance in these seals was demonstrated by arterial P-O2 values during late apnea that were less than human thresholds for shallow-water blackout. Despite such low P-O2s, there was no evidence of significant anaerobic metabolism, as changes in blood pH were minimal and attributable to increased P-CO2. These findings and the previously reported lack of lactate accumulation during these breath- holds are consistent with the maintenance of aerobic metabolism even at low oxygen tensions during rest- associated apneas. Such hypoxemic tolerance is necessary in order to allow dissociation of O-2 from hemoglobin and provide effective utilization of the blood O-2 store.

2002
Ponganis, PJ, Kreutzer U, Sailasuta N, Knower T, Hurd R, Jue T.  2002.  Detection of myoglobin desaturation in Mirounga angustirostris during apnea. American Journal of Physiology-Regulatory Integrative and Comparative Physiology. 282:R267-R272. AbstractWebsite

H-1 NMR solution-state study of elephant seal (Mirounga angustirostris) myoglobin (Mb) and hemoglobin (Hb) establishes the temperature-dependent chemical shifts of the proximal histidyl NdeltaH signal, which reflects the respective intracellular and vascular PO2 in vivo. Both proteins exist predominantly in one major isoform and do not exhibit any conformational heterogeneity. The Mb and Hb signals are detectable in M. angustirostris tissue in vivo. During eupnea M. angustirostris muscle maintains a well-saturated MbO(2). However, during apnea, the deoxymyoglobin proximal histidyl NdeltaH signal becomes visible, reflecting a declining tissue PO2. The study establishes a firm methodological basis for using NMR to investigate the metabolic responses during sleep apnea of the elephant seal and to secure insights into oxygen regulation in diving mammals.

2001
Nagy, KA, Kooyman GL, Ponganis PJ.  2001.  Energetic cost of foraging in free-diving emperor penguins. Physiological and Biochemical Zoology. 74:541-547.   10.1086/322165   AbstractWebsite

Hypothesizing that emperor penguins (Aptenodytes forsteri) would have higher daily energy expenditures when foraging for their food than when being hand-fed and that the increased expenditure could represent their foraging cost, we measured field metabolic rates (FMR; using doubly labeled water) over 4-d periods when 10 penguins either foraged under sea ice or were not allowed to dive but were fed fish by hand. Surprisingly, penguins did not have higher rates of energy expenditure when they dove and captured their own food than when they did not forage but were given food. Analysis of time-activity and energy budgets indicated that FMR was about 1.7 x BMR (basal metabolic rate) during the 12 h d(-1) that penguins were lying on sea ice. During the remaining 12 h d(-1), which we termed their "foraging period" of the day, the birds were alert and active (standing, preening, walking, and either free diving or being hand-fed), and their FMR was about 4.1 x BMR. This is the lowest cost of foraging estimated to date among the eight penguin species studied. The calculated aerobic diving limit (ADL(C)), determined with the foraging period metabolic rate of 4.1 x BMR and known O-2 stores, was only 2.6 min, which is far less than the 6-min ADL previously measured with postdive lactate analyses in emperors diving under similar conditions. This indicates that calculating ADL(C) from an at-sea or foraging-period metabolic rate in penguins is not appropriate. The relatively low foraging cost for emperor penguins contributes to their relatively low total daily FMR (2.9 x BMR). The allometric relationship for FMR in eight penguin species, including the smallest and largest living representatives, is kJ d(-1) = 1,185 kg(0.705).

1999
Dolar, MLL, Suarez P, Ponganis PJ, Kooyman GL.  1999.  Myoglobin in pelagic small cetaceans. Journal of Experimental Biology. 202:227-236. AbstractWebsite

Although myoglobin (Mb) is considered to contribute significantly to the oxygen and diving capacity of marine mammals, few data are available for cetaceans, Cetacean by-catch in the tuna driftnet fisheries in the Sulu Sea, Philippines, afforded the opportunity to examine Mb content and distribution, and to determine muscle mass composition, in Fraser's (Lagenodelphis hosei) and spinner (Stenella longirostris) dolphins and a pygmy killer whale (Feresa attenuata). Age was estimated by body length determination. Stomach contents were analyzed for the presence or absence of milk and solid foods. It was hypothesized (a) that Mb concentration ([Mb]) would be higher in Fraser's and spinner dolphins than in other small cetaceans because of the known mesopelagic distribution of their prey, (b) that [Mb] would vary among different muscles according to function during diving, and (c) that [Mb] would increase with age during development. The results were as follows. ii) Myoglobin concentrations of the longissimus muscle in adult Fraser's (6.8-7.2 g 100 g(-1) muscle) and spinner (5-6 g 100 g(-1) muscle) dolphins and in an immature pygmy killer whale (5.7 g 100 g(-1) muscle) were higher than those reported previously for small cetaceans, (2) [Mb] varied significantly among the different muscle types in adult dolphins but not in calves; in adults, swimming muscles had significantly higher [Mb] than did non-swimming muscles, contained 82-86 % of total Mb, and constituted 75-80 % of total muscle mass. (3) Myoglobin concentrations in Fraser's and spinner dolphins increased with size and age and were 3-4 times greater in adults than in calves, The high Mb concentrations measured in the primary locomotory muscles of these pelagic dolphins are consistent with the known mesopelagic foraging behaviour of Fraser's and spinner dolphins and suggest that the pygmy killer whale is also a deep-diving species. The high Mb concentrations in epaxial, hypaxial and abdominal muscle groups also support the primary locomotory functions suggested for these muscles in other anatomical studies. As in other species. the increase in [Mb] during development probably parallels the development of diving capacity.

1998
Kooyman, GL, Ponganis PJ.  1998.  The physiological basis of diving to depth: Birds and mammals. Annual Review of Physiology. 60:19-32.   10.1146/annurev.physiol.60.1.19   AbstractWebsite

There is wide diversity in the animals that dive to depth and in the distribution of their body oxygen stores. A hallmark of animals diving to depth is a substantial elevation of muscle myoglobin concentration. In deep divers, more than 80% of the oxygen store is in the blood and muscles. How these oxygen stores are managed, particularly within muscle, is unclear. The aerobic endurance of four species has now been measured. These measurements provide a standard for other species in which the limits cannot be measured. Diving to depth requires several adaptations to the effects of pressure. In mammals, one adaptation is lung collapse at shallow depths, which limits absorption of nitrogen. Blood Nz levels remain below the threshold for decompression sickness. No such adaptive model is known for birds. There appear to be two diving strategies used by animals that dive to depth. Seals, for example, seldom rely on anaerobic metabolism. Birds, on the other hand, frequently rely on anaerobic metabolism to exploit prey-rich depths otherwise unavailable to them.

1997
Kooyman, GL, Ponganis PJ.  1997.  The challenges of diving to depth. American Scientist. 85:530-539. AbstractWebsite
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Ponganis, PJ, Kooyman GL, Starke LN, Kooyman CA, Kooyman TG.  1997.  Post-dive blood lactate concentrations in emperor penguins, Aptenodytes forsteri. Journal of Experimental Biology. 200:1623-1626. AbstractWebsite

In order to determine an aerobic diving limit (ADL) in emperor penguins (Aptenodytes forsteri), post-dive blood lactate concentrations were measured in penguins foraging at an isolated sea ice hole. Resting lactate concentrations were 1.2-2.7 mmol l(-1). Serial samples revealed that lactate level usually peaked within 5 min after dives and that 7-12 min was required for lactate concentrations to decrease from 5-8 mmol l(-1) to less than 2.5 mmol l(-1). Post-dive lactate level was not elevated above 3 mmol l(-1) for dives shorter than 5 min. Two-phase regression analysis revealed a transition at 5.6 min in the post-dive lactate level versus diving duration relationship. All dives longer than 7 min were associated with lactate concentrations greater than 5 mmol l(-1). We conclude that the ADL in emperor penguins ranges between 5 and 7 min. These are the first determinations of post-dive lactate concentrations in any free-diving bird and are currently the only physiological assessment of an ADL in an avian species.

Ponganis, PJ, Kooyman GL, Winter LM, Starke LN.  1997.  Heart rate and plasma lactate responses during submerged swimming and trained diving in California sea lions, Zalophus californianus. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology. 167:9-16.   10.1007/s003600050042   AbstractWebsite

California sea lions, Zalophus californianus, were trained to elicit maximum voluntary breath holds during stationary underwater targeting, submerged swimming, and trained diving. Lowest heart rate during rest periods was 57 bpm. The heart rate profiles in all three protocols were dominated by a bradycardia of 20-50 bpm, and demonstrated that otariid diving heart rates were at or below resting heart rate. Venous blood samples were collected after submerged swimming periods of 1-3 min. Plasma lactate began to increase only after 2.3-min submersions. This rise in lactate and our inability to train sea lions to dive or swim submerged for periods longer than 3 min lead us to conclude that an aerobic limit had been reached. Due to the similarity of heart rate responses and swimming velocities recorded during submerged swimming and trained diving, this 2.3-min limit should approximate the aerobic dive limit in these 40-kg sea lions. Total body O-2 stores, based on measurements of blood and muscle O-2 stores in these animals, and prior lung O-2 Store analyses, were 37-43 ml O-2 kg(-1). The aerobic dive limit, calculated with these O-2 stores and prior measurements of at-sea metabolic rates of sea lions, is 1.8-2 min, similar to that measured by the change in post-submersion lactate concentration.

Ponganis, PJ, Kooyman GL, Baranov EA, Thorson PH, Stewart BS.  1997.  The aerobic submersion limit of Baikal seals, Phoca sibirica. Canadian Journal of Zoology-Revue Canadienne De Zoologie. 75:1323-1327.   10.1139/z97-756   AbstractWebsite

An aerobic dive limit (ADL), the diving duration beyond which postdive lactate concentration increases above the resting level, has been estimated theoretically for many species. Such calculations have been based on an oxygen store/diving metabolic rate (MR) equation. Until now, an ADL has been determined empirically from measurements of blood lactate concentration only in the Weddell seal, Leptonychotes weddellii. We measured post-submergence plasma lactate concentrations during spontaneous voluntary submersions of three captive adult Baikal seals (Phoca sibirica). Two-phase regression analysis revealed a transition in the lactate concentration - submersion duration relationship after the animal had been diving for 15 min. Data collected in prior studies on oxygen stores and submersion metabolic rates of Baikal seals yielded a calculated aerobic limit of 16 min. As in Weddell seals, the empirically determined aerobic limit was very similar to the theoretical limit. Furthermore, most diving durations recorded during recent studies of free-ranging Baikal seals are under this limit. These data support the concept of an ADL and its estimation by means of an oxygen store/diving MR calculation.

1992
Ponganis, PJ, Gentry RL, Ponganis EP, Ponganis KV.  1992.  Analysis of swim velocities during deep and shallow dives of two northern fur seals, Callorhinus ursinus. Marine Mammal Science. 8:69-75.   10.1111/j.1748-7692.1992.tb00126.x   AbstractWebsite

Swim velocities at 15-sec intervals and maximum depth per dive were recorded by microprocessor units on two "mixed diver" adult female northern fur seals during summer foraging trips. These records allowed comparison of swim velocities of deep (> 75 m) and shallow (< 75 m) dives. Deep dives averaged 120 m depth and 3 min duration; shallow dives averaged 30 m and 1.2 min. Mean swim velocities on deep dives were 1.8 and 1.5 m/ sec for the two animals; mean swim velocities on shallow dives were 1.5 and 1.2 m/sec. The number of minutes per hour spent diving during the deep and shallow dive patterns were 11 and 27 min, respectively. Swim velocity, and hence, relative metabolic rate, did not account for the differences in dive durations between deep and shallow dives. The long surface durations associated with deep dives, and estimates of metabolic rates for the observed swim velocities, suggest that deep dives involve significant anaerobic metabolism.

Ponganis, PJ, Kooyman GL, Sartoris D, Jobsis P.  1992.  Pinniped splenic volumes. American Journal of Physiology. 262:R322-R325. AbstractWebsite

Splenic volume was measured by computerized axial tomography in three harbor seals (Phoca vitulina) and two California sea lions (Zalophus californianus). Volumes ranged from 228 to 679 ml, representing 0.8-3.0% of calculated percentage body mass. Despite possible variation in the state of splenic contraction during the examination, these values are in the upper range of reported mammalian splenic volumes (as % of body mass). This reinforces the pinniped splenic erythrocyte storage concept.