Extreme hypoxemic tolerance and blood oxygen depletion in diving elephant seals

Abstract

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.

Lung collapse in the diving sea lion: hold the nitrogen and save the oxygen

“…A P O2 electrode was placed percutaneously in the aorta [8,14] and connected via a waterproof cable to a custom built microprocessor P O2 data logger mounted dorsally midline above the hips. Additionally, a time-depth recorder (TDR) and a radio transmitter were mounted above the logger.…”

“…Depths of lung collapse in the pressure chamber studies were variable and, at least partially, dependent on inhaled air volume [3,4,7]. In free-diving elephant seals, arterial partial pressure of oxygen ðP O 2 Þ profiles revealed that P O 2 continued to increase in some dives at depths as deep as 83 m, consistent with increased inhaled air volumes and maintenance of gas exchange to greater depths in such dives [8]. Recent modelling suggests that depth of lung collapse in seals and dolphins may be much deeper than estimated in earlier field studies [9,10].…”

Physiological constraints and energetic costs of diving behaviour in marine mammals: a review of studies using trained Steller sea lions diving in the open ocean

“…The blood PO2 of marine mammals can reach levels below that typically exhibited by 642 terrestrial counterparts (Meir et al 2009). At the same time, the blood of marine 643 mammals can carry more CO2 as carboxyhemoglobin than terrestrial mammals (Tift 644 et al 2014), and they may be more tolerant of higher PCO2 levels and better able to 645 buffer its effects (Castellini 1991; Lenfant et al 1970).…”

Characterization of the hypoxia-inducible factor 1 alpha gene in the sperm whale, beluga whale, and Yangtze finless porpoise

“…The 742nd amino acid is the same (Thr) in the sperm whale, beluga whale, and elephant seal, but it is Ala in the Yangtze finless porpoise and mole rat. The elephant seal, the most well-demonstrated diving marine animal, routinely tolerates extreme hypoxemia during dives to completely utilize the blood O 2 store and maximize aerobic dive duration (Meir et al 2009). The full-length cDNA sequences of three HIF-α isoforms were identified and characterized from northern elephant seal muscle (Soñanez-Organis et al 2013).…”