Muscle Energy Stores and Stroke Rates of Emperor Penguins: Implications for Muscle Metabolism and Dive Performance

Abstract

In diving birds and mammals, bradycardia and peripheral vasoconstriction potentially isolate muscle from the circulation. During complete ischemia, ATP production is dependent on the size of the myoglobin oxygen (O2) store and the concentrations of phosphocreatine (PCr) and glycogen (Gly). Therefore, we measured PCr and Gly concentrations in the primary underwater locomotory muscle of emperor penguin and modeled the depletion of muscle O2 and those energy stores under conditions of complete ischemia and a previously determined muscle metabolic rate. We also analyzed stroke rate to assess muscle workload variation during dives and evaluate potential limitations on the model. Measured PCr and Gly concentrations, 20.8 and 54.6 mmol kg−1, respectively, were similar to published values for non-diving animals. The model demonstrated that PCr and Gly provide a large anaerobic energy store, even for dives longer than 20 min. Stroke rate varied throughout the dive profile indicating muscle workload was not constant during dives as was assumed in the model. The stroke rate during the first 30 seconds of dives increased with increased dive depth. In extremely long dives, lower overall stroke rates were observed. Although O2 consumption and energy store depletion may vary during dives, the model demonstrated that PCr and Gly, even at concentrations typical of terrestrial birds and mammals, are a significant anaerobic energy store and can play an important role in the emperor penguin’s ability to perform long dives.

Penguin lungs and air sacs: implications for baroprotection, oxygen stores and buoyancy

“…Although such buoyancies, especially for king and emperor penguins, are higher than typically estimated for small penguins, buoyancy is greater in larger animals (Miller et al, 2004;Skrovan et al, 1999), and emperor and king penguins are much larger birds than those other avian species in which buoyancy has been previously estimated. In addition, greater buoyancy could probably be rapidly diminished by a quicker descent and faster stroke rate at the start of deeper dives (Williams et al, 2012). Lastly, field observations of floating penguins (Fig.…”

Metabolism at the Max: How Vertebrate Organisms Respond to Physical Activity

“…ATP concentrations within red and white skeletal muscle fibers from vertebrates (see Refs. 6,11,27,36,56,72,119,146,157,160,164,177,182,200,202,207,219,243,256,265,269,293,294,308). For mammals, red vs. white [CP], P = 0.0006 (two-tailed t test); for all vertebrates combined, red versus white [CP], P = 0.0085 (two-tailed t test).…”

The dive performance of immature king penguins following their annual molt suggests physiological constraints

“…A longer recovery period at the surface might also have been the consequence of an increased contribution of anaerobic metabolism (especially phosphocreatine, PCr) during diving. While reliance on anaerobic metabolism might be limited to extended dives (Baldwin et al, 1984;Baldwin, 1988;Ponganis et al, 1997d), PCr recovery might be similarly fast as Mb-O 2 recovery (Williams et al, 2012). For emperor penguins, which possess a large anaerobic energy reserve in form of glycogen and PCr in their pectoral muscles, it was suggested that Mb-O 2 and PCr recovery should occur within most observed post-dive surface intervals (Williams et al, 2012).…”

“…While reliance on anaerobic metabolism might be limited to extended dives (Baldwin et al, 1984;Baldwin, 1988;Ponganis et al, 1997d), PCr recovery might be similarly fast as Mb-O 2 recovery (Williams et al, 2012). For emperor penguins, which possess a large anaerobic energy reserve in form of glycogen and PCr in their pectoral muscles, it was suggested that Mb-O 2 and PCr recovery should occur within most observed post-dive surface intervals (Williams et al, 2012). A stronger depletion of the reduced oxygen stores during post-molt (and/or a potential increase in anaerobic metabolism) could be the consequence of an increased work load to generate sufficient heat so that the presumably high heat loss can be balanced and core temperature is maintained (see discussion on vertical speed changes below).…”

“…However, a switch to anaerobic metabolism will increase recovery times at the surface between dives and reduce dive efficiency (Kooyman et al, 1980;Ponganis et al, 1997a,b,c), and might, therefore, be restricted to extended dives and short swimming bursts (Baldwin et al, 1984;Baldwin, 1988;Ponganis et al, 1997d). In addition, the anaerobic energy store of the pectoral muscle ( phosphocreatine and glycogen; Williams et al, 2012) will also be curtailed after substantial muscle mass loss during molt, further reducing the potential for ATP production.…”