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2013
Meir, JU, Robinson PW, Vilchis LI, Kooyman GL, Costa DP, Ponganis PJ.  2013.  Blood oxygen depletion is independent of dive function in a deep diving vertebrate, the northern elephant seal. Plos One. 8   10.1371/journal.pone.0083248   AbstractWebsite

Although energetics is fundamental to animal ecology, traditional methods of determining metabolic rate are neither direct nor instantaneous. Recently, continuous blood oxygen (O-2) measurements were used to assess energy expenditure in diving elephant seals (Mirounga angustirostris), demonstrating that an exceptional hypoxemic tolerance and exquisite management of blood O-2 stores underlie the extraordinary diving capability of this consummate diver. As the detailed relationship of energy expenditure and dive behavior remains unknown, we integrated behavior, ecology, and physiology to characterize the costs of different types of dives of elephant seals. Elephant seal dive profiles were analyzed and O-2 utilization was classified according to dive type (overall function of dive: transit, foraging, food processing/rest). This is the first account linking behavior at this level with in vivo blood O-2 measurements in an animal freely diving at sea, allowing us to assess patterns of O-2 utilization and energy expenditure between various behaviors and activities in an animal in the wild. In routine dives of elephant seals, the blood O-2 store was significantly depleted to a similar range irrespective of dive function, suggesting that all dive types have equal costs in terms of blood O-2 depletion. Here, we present the first physiological evidence that all dive types have similarly high blood O-2 demands, supporting an energy balance strategy achieved by devoting one major task to a given dive, thereby separating dive functions into distinct dive types. This strategy may optimize O-2 store utilization and recovery, consequently maximizing time underwater and allowing these animals to take full advantage of their underwater resources. This approach may be important to optimizing energy expenditure throughout a dive bout or at-sea foraging trip and is well suited to the lifestyle of an elephant seal, which spends >90% of its time at sea submerged making diving its most "natural" state.

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.

2008
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.

2007
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.  2007.  Bio-logging of physiological parameters in higher marine vertebrates. Deep-Sea Research Part Ii-Topical Studies in Oceanography. 54:183-192.   10.1016/j.dsr2.2006.11.009   AbstractWebsite

Bio-logging of physiological parameters in higher marine vertebrates had its origins in the field of bio-telemetry in the 1960s and 1970s. The development of microprocessor technology allowed its first application to bio-logging investigations of Weddell seal diving physiology in the early 1980s. Since that time, with the use of increased memory capacity, new sensor technology, and novel data processing techniques, investigators have examined heart rate, temperature, swim speed, stroke frequency, stomach function (gastric pH and motility), heat flux, muscle oxygenation, respiratory rate, diving air volume, and oxygen partial pressure (PO(2)) during diving. Swim speed, heart rate, and body temperature have been the most commonly studied parameters. Bio-logging investigation of pressure effects has only been conducted with the use of blood samplers and nitrogen analyses on animals diving at isolated dive holes. The advantages/disadvantages and limitations of recording techniques, probe placement, calibration techniques, and study conditions are reviewed. (c) 2007 Elsevier Ltd. All rights reserved.

1990
Kooyman, G, Ponganis PJ.  1990.  Behavior and physiology of diving in emperor and king penguins. Penguin biology. ( Davis L, Darby JT, Eds.).:14., San Diego: Academic Press Abstract
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