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Understanding the aerobic dive limit and dive performance of emperor penguins : muscle oxygen depletion patterns and anaerobic energy reserves

Abstract

Isolation of muscle from the circulation, depletion of the muscle oxygen store and subsequent anaerobic metabolism has been postulated as the physiological basis for the aerobic dive limit (ADL). During complete ischemia, energy production is dependent on the size of the myoglobin oxygen (Mb-O₂) store and phosphocreatine (PCr) and glycogen (Gly) concentrations. A dual wavelength near- infrared spectrophotometer was developed and used to measure myoglobin (Mb) O₂ saturation levels in the locomotory muscle during dives of emperor penguins (Aptenodytes forsteri). PCr and Gly concentrations in emperor penguin muscle were measured and the depletion of muscle O₂ and those energy stores were modeled under conditions of complete ischemia. Stroke frequency was also analyzed to assess muscle workload during dives and potential effects on the model. Two distinct patterns of muscle O₂ depletion were observed. Type A dives had a monotonic decline, and, in dives near the ADL, the muscle O₂ store was almost completely depleted. This pattern of Mb desaturation was consistent with lack of muscle blood flow and supports the hypothesis that muscle O₂ depletion triggers the ADL. A mean muscle O₂ consumption of 12.4 ml O₂ kg⁻¹ muscle min⁻¹ and a diving O₂ consumption of 6.8 ml O₂ kg⁻¹ were calculated. Type B desaturation patterns demonstrated a more gradual decline, often reaching a mid- dive plateau in Mb desaturation. This pattern suggests maintenance of some muscle perfusion during these dives. Measured PCr and Gly concentrations, 20.8 and 54.6 mmol kg⁻¹ muscle, respectively, were similar to those in non- diving animals. Although stroke frequency was not constant during dives, as was assumed in the model, the model demonstrated that PCr and Gly provide a large anaerobic energy store that can contribute significantly to the penguin's ability to perform long dives. These results demonstrate that emperor penguins (1) can either isolate muscle from the circulation during dives or perfuse muscle to supplement the muscle O₂ store, (2) have low muscle and total body diving oxygen consumption rates, and (3) have normal PCr and Gly concentrations, which provide significant anaerobic energy stores

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