Paul J. Ponganis

Determinants of the Aerobic Dive Limit of Weddell Seals: Analysis of Diving Metabolic Rates, Postdive End Tidal Po2's, and Blood and Muscle Oxygen Stores

The mean aerobic dive limit (ADL) for Weddell seals was calculated from data collected on diving metabolic rates (V̇o2) and blood and muscle O₂ stores. Mean diving V̇o2 of adult seals during predominantly exploratory dive patterns was 4.5 mL O2 kg−1 min−1; mean V̇o2 of a subadult seal engaged in foraging dive bouts was 8.5 mL O2 kg−1 min−1. The adult value was 30% greater than that used in past ADL calculations. Mean plasma volume was 7% body mass (BM); blood volume calculated with the highest hematocrit (Hct) observed (66) was 21% BM. Hemoglobin concentration at such an Hct was 26% by weight. End tidal Po2 (pre-and postdive) justified the use of 95% and 20% arterial O2 saturations in the blood O2 store calculation. Total blood O2 stores were 50% greater than those used in past ADL calculations. Mean myoglobin concentration (5.4% by weight) and more recent anatomical estimates of muscle mass yielded a 35% increase in muscle O2 stores. The mean estimated ADL for a 450-kg seal calculated with these new data was 19.1 min, 2.3 min greater than in past calculations and only 1 min less than the 20-min inflection point of the curve of dive duration versus postdive lactic acid appearance. For the subadult engaged in foraging dives, the mean estimated ADL was about 9 min, again quite similar to past ADL calculations.

Stroke frequency, but not swimming speed, is related to body size in free-ranging seabirds, pinnipeds and cetaceans

It is obvious, at least qualitatively, that small animals move their locomotory apparatus faster than large animals: small insects move their wings invisibly fast, while large birds flap their wings slowly. However, quantitative observations have been difficult to obtain from free-ranging swimming animals. We surveyed the swimming behaviour of animals ranging from 0.5 kg seabirds to 30 000 kg sperm whales using animal-borne accelerometers. Dominant stroke cycle frequencies of swimming specialist seabirds and marine mammals were proportional to mass−0.29 (R2=0.99, n=17 groups), while propulsive swimming speeds of 1–2 m s−1 were independent of body size. This scaling relationship, obtained from breath-hold divers expected to swim optimally to conserve oxygen, does not agree with recent theoretical predictions for optimal swimming. Seabirds that use their wings for both swimming and flying stroked at a lower frequency than other swimming specialists of the same size, suggesting a morphological trade-off with wing size and stroke frequency representing a compromise. In contrast, foot-propelled diving birds such as shags had similar stroke frequencies as other swimming specialists. These results suggest that muscle characteristics may constrain swimming during cruising travel, with convergence among diving specialists in the proportions and contraction rates of propulsive muscles.

Extreme hypoxemic tolerance and blood oxygen depletion in diving elephant seals

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(O(2)) and Pa(O(2)) 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 Pa(O(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.

Heart rate and plasma lactate responses during submerged swimming and trained diving in California sea lions, Zalophus californianus

Abstract 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 O2 stores, based on measurements of blood and muscle O2 stores in these animals, and prior lung O2 store analyses, were 37–43 ml O2 kg−1. The aerobic dive limit, calculated with these O2 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.

In pursuit of Irving and Scholander: a review of oxygen store management in seals and penguins

Summary Since the introduction of the aerobic dive limit (ADL) 30 years ago, the concept that most dives of marine mammals and sea birds are aerobic in nature has dominated the interpretation of their diving behavior and foraging ecology. Although there have been many measurements of body oxygen stores, there have been few investigations of the actual depletion of those stores during dives. Yet, it is the pattern, rate and magnitude of depletion of O2 stores that underlie the ADL. Therefore, in order to assess strategies of O2 store management, we review (a) the magnitude of O2 stores, (b) past studies of O2 store depletion and (c) our recent investigations of O2 store utilization during sleep apnea and dives of elephant seals (Mirounga angustirostris) and during dives of emperor penguins (Aptenodytes forsteri). We conclude with the implications of these findings for (a) the physiological responses underlying O2 store utilization, (b) the physiological basis of the ADL and (c) the value of extreme hypoxemic tolerance and the significance of the avoidance of re-perfusion injury in these animals.

Regional heterothermy and conservation of core temperature in emperor penguins diving under sea ice

Temperatures were recorded at several body sites in emperor penguins (Aptenodytes forsteri) diving at an isolated dive hole in order to document temperature profiles during diving and to evaluate the role of hypothermia in this well-studied model of penguin diving physiology. Grand mean temperatures (+/-S.E.) in central body sites during dives were: stomach: 37.1+/-0.2 degrees C (n=101 dives in five birds), pectoral muscle: 37.8+/-0.1 degrees C (n=71 dives in three birds) and axillary/brachial veins: 37.9+/-0.1 degrees C (n=97 dives in three birds). Mean diving temperature and duration correlated negatively at only one site in one bird (femoral vein, r=-0.59, P<0.05; range <1 degrees C). In contrast, grand mean temperatures in the wing vein, foot vein and lumbar subcutaneous tissue during dives were 7.6+/-0.7 degrees C (n=157 dives in three birds), 20.2+/-1.2 degrees C (n=69 in three birds) and 35.2+/-0.2 degrees C (n=261 in six birds), respectively. Mean limb temperature during dives negatively correlated with diving duration in all six birds (r=-0.29 to -0.60, P<0.05). In two of six birds, mean diving subcutaneous temperature negatively correlated with diving duration (r=-0.49 and -0.78, P<0.05). Sub-feather temperatures decreased from 31 to 35 degrees C during rest periods to a grand mean of 15.0+/-0.7 degrees C during 68 dives of three birds; mean diving temperature and duration correlated negatively in one bird (r=-0.42, P<0.05). In general, pectoral, deep venous and even stomach temperatures during diving reflected previously measured vena caval temperatures of 37-39 degrees C more closely than the anterior abdominal temperatures (19-30 degrees C) recently recorded in diving emperors. Although prey ingestion can result in cooling in the stomach, these findings and the lack of negative correlations between internal temperatures and diving duration do not support a role for hypothermia-induced metabolic suppression of the abdominal organs as a mechanism of extension of aerobic dive time in emperor penguins diving at the isolated dive hole. Such high temperatures within the body and the observed decreases in limb, anterior abdomen, subcutaneous and sub-feather temperatures are consistent with preservation of core temperature and cooling of an outer body shell secondary to peripheral vasoconstriction, decreased insulation of the feather layer, and conductive/convective heat loss to the water environment during the diving of these emperor penguins.

Heart rate regulation and extreme bradycardia in diving emperor penguins

SUMMARY To investigate the diving heart rate (fH) 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<fH at rest) occurred during diving [dive fH (total beats/duration)=57±2 beats min–1, fH 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 fH=85±3 beats min–1, whereas fH in dives greater than the ADL was significantly lower (41±1 beats min–1). In dives greater than the ADL, fH reached extremely low values: fH during the last 5 mins of an 18 min dive was 6 beats min–1. Dive fH and minimum instantaneous fH during dives declined significantly with increasing dive duration. Dive fH 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 fH in this study is the highest ever recorded for emperor penguins (256 beats min–1), equivalent to fH at V̇O2 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.

High-affinity hemoglobin and blood oxygen saturation in diving emperor penguins

SUMMARY The emperor penguin (Aptenodytes forsteri) thrives in the Antarctic underwater environment, diving to depths greater than 500 m and for durations longer than 23 min. To examine mechanisms underlying the exceptional diving ability of this species and further describe blood oxygen (O2) transport and depletion while diving, we characterized the O2–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 O2 depletion during diving, by applying the dissociation curve to previously collected partial pressure of O2 (PO2) profiles to estimate in vivo Hb saturation (SO2) changes during dives. This investigation revealed enhanced Hb–O2 affinity (P50=28 mmHg, pH 7.5) in the emperor penguin, similar to high-altitude birds and other penguin species. This allows for increased O2 at low blood PO2 levels during diving and more complete depletion of the respiratory O2 store. SO2 profiles during diving demonstrated that arterial SO2 levels are maintained near 100% throughout much of the dive, not decreasing significantly until the final ascent phase. End-of-dive venous SO2 values were widely distributed and optimization of the venous blood O2 store resulted from arterialization and near complete depletion of venous blood O2 during longer dives. The estimated contribution of the blood O2 store to diving metabolic rate was low and highly variable. This pattern is due, in part, to the influx of O2 from the lungs into the blood during diving, and variable rates of tissue O2 uptake.

Returning on empty: extreme blood O2 depletion underlies dive capacity of emperor penguins.

SUMMARY Blood gas analyses from emperor penguins (Aptenodytes forsteri) at rest, and intravascular PO2 profiles from free-diving birds were obtained in order to examine hypoxemic tolerance and utilization of the blood O2 store during dives. Analysis of blood samples from penguins at rest revealed arterial PO2s and O2 contents of 68±7 mmHg (1 mmHg= 133.3 Pa) and 22.5±1.3 ml O2 dl–1 (N=3) and venous values of 41±10 mmHg and 17.4±2.9 ml O2 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 PO2 profiles obtained from birds equipped with intravascular PO2 electrodes and backpack recorders during dives revealed that (1) the decline of the final blood PO2 of a dive in relation to dive duration was variable, (2) final venous PO2 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 PO2 values were indistinguishable in longer dives, and (4) final venous PO2 values of longer dives were as low as 1–6 mmHg during dives. Although blood O2 is not depleted at the ADL, nearly complete depletion of the blood O2 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 O2–Hb dissociation curve of the emperor penguin in comparison to those of most birds. A relatively higher-affinity Hb is consistent with blood PO2 values and O2 contents of penguins at rest.

Blood flow and metabolic regulation in seal muscle during apnea

SUMMARY 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 t1/2 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 O2 depletion rate of 1–2.3 ml O2 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 4.5×10–7 cm2 s–1, consistent with the value observed in rat myocardium. Equipoise PO2 analysis revealed that Mb is the predominant intracellular O2 transporter in elephant seals during eupnea and apnea.