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Journal Article
Knower Stockard, T, Heil J, Meir JU, Sato K, Ponganis KV, Ponganis PJ.  2005.  Air sac P-O2 and oxygen depletion during dives of emperor penguins. Journal of Experimental Biology. 208:2973-2980.   10.1242/jeb.01687   AbstractWebsite

In order to determine the rate and magnitude of respiratory O-2 depletion during dives of emperor penguins (Aptenodytes forsteri), air sac O-2 partial pressure (PO2) was recorded in 73 dives of four birds at an isolated dive hole. These results were evaluated with respect to hypoxic tolerance, the aerobic dive limit (ADL; dive duration beyond which there is post-dive lactate accumulation) and previously measured field metabolic rates (FMRs). 55% of dives were greater in duration than the previously measured 5.6-min ADL. P-O2 and depth profiles revealed compression hyperoxia and gradual O-2 depletion during dives. 42% of final P(O2)s during the dives (recorded during the last 15 s of ascent) were < 20 mmHg (< 2.7 kPa). Assuming that the measured air sac P-O2 is representative of the entire respiratory system, this implies remarkable hypoxic tolerance in emperors. In dives of durations greater than the ADL, the calculated end-of-dive air sac O-2 fraction was < 4%. The respiratory O-2 store depletion rate of an entire dive, based on the change in O-2 fraction during a dive and previously measured diving respiratory volume, ranged from I to 5 ml O-2 kg(-1) min(-1) and decreased exponentially with diving duration. The mean value, 2.1 +/- 0.8 ml O-2 kg(-1) min(-1), was (1) 19-42% of previously measured respiratory O-2 depletion rates during forced submersions and simulated dives, (2) approximately one-third of the predicted total body resting metabolic rate and (3) approximately 10% of the measured FMR. These findings are consistent with a low total body metabolic rate during the dive.

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.

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.

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.

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.

Ponganis, PJ, Costello ML, Starke LN, MathieuCostello O, Kooyman GL.  1997.  Structural and biochemical characteristics of locomotory muscles of emperor penguins, Aptenodytes forsteri. Respiration Physiology. 109:73-80.   10.1016/s0034-5687(97)84031-5   AbstractWebsite

Structural and biochemical characteristics of the primary muscles used for swimming (pectoralis, PEC and supracoracoideus, SC) were compared to those of leg muscles in emperor penguins (Aptenodytes forsteri). The mass of PEG-SC was four times that of the leg musculature, and mitochondrial volume density in PEC and SC (4%) was two-thirds that in sartorius (S) and gastrocnemius. The differences in muscle mass and mitochondrial density yielded a 2.2-fold greater total mitochondrial content in PEG-SC than leg muscles, which appears to account for the 1.8-fold greater whole-body highest oxygen consumption previously recorded in emperor penguins during swimming compared to walking. Calculation of maximal mitochondrial O-2 consumption in PEG-SC and leg muscle yielded values of 5.8-6.9 mi O-2 ml(-1) min(-1), which are similar to those in locomotory muscles of most mammals and birds. A distinct feature of emperor penguin muscle was its myoglobin content, with concentrations in PEG-SC (6.4 g 100 g(-1)) among the highest measured in any species. This resulted in a PEG-SC O-2 store greater than that of the entire blood. In addition, ratios of myoglobin content to mitochondrial volume density and to citrate synthase activity were 4.4 and 2.5 times greater in PEG than in S, indicative of the significant role of myoglobin in the adaptation of muscle to cardiovascular adjustments during diving. (C) 1997 Elsevier Science B.V.