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Impacts of carbon monoxide (CO) and muscle workload on oxygen utilization in marine mammals

Abstract

For air-breathing divers, oxygen stores represent crucial resources for survival. The primary oxygen store for deep-diving animals is the blood oxygen store, which is typically enlarged in diving species and is mainly comprised of hemoglobin. Efficient utilization of blood oxygen stores while diving is critical for the optimization of dive durations. During dives, animals exhibit the dive response which is a reduction in both heart rate and blood flow to peripheral tissues. However, animals also must increase muscle workload (swim) to reach depths and to return to the surface from a dive, which has the potential to interfere with heart rate and blood oxygen use during dives. The erythrocytes that carry hemoglobin have a limited lifespan, and are constantly turned over in the body. The destruction of erythrocytes releases hemoglobin into circulation, where the heme portion of hemoglobin is degraded by heme oxygenase enzymes, and results in equimolar production of carbon monoxide (CO). Increased hemoglobin stores of marine mammals make them susceptible to elevated CO production. Due to the high affinity of hemoglobin for CO over oxygen, increased endogenous CO production could impact blood oxygen stores.

In this dissertation, I address the effect of muscle workload and endogenous CO on blood oxygen use in marine mammals. I highlight the lack of relationship between muscle workload and posterior vena caval oxygen depletion during deep dives of free-ranging California sea lions. I hypothesize this is a reflection of the extreme posterior peripheral vasoconstriction associated with the dive response. I also present the variation in flipper stroke rate patterns in sea lions, with prolonged glides during the descent and ascent of deep dives. I show that species with elevated hemoglobin stores (elephant seals and beluga whales) exhibit increased endogenous CO production. In adult elephant seals, this results in over 10% of hemoglobin stores being bound to CO. These levels of CO shift the oxygen-hemoglobin dissociation curve to the left, increasing hemoglobin-oxygen affinity, and increases oxygen content at the end of dives. This is the first report of endogenous CO leading to increased hemoglobin-oxygen affinity in a species adapted to tolerate chronic hypoxia.

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