What triggers the aerobic dive limit? Patterns of muscle oxygen depletion during dives of emperor penguins

Williams, C. L.; Meir, Jessica U.; Ponganis, Paul J.

doi:10.1242/jeb.052233

Cited by 54 publications

(83 citation statements)

References 68 publications

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“…Such plasticity in blood flow distribution has also been observed in diving emperor penguins (Williams et al, 2011). Max.…”

Section: Discussion Flipper Stroke Patternssupporting

confidence: 52%

“…The severe bradycardia and peripheral vasoconstriction observed in the classic dive response conserves oxygen in blood by directing it towards hypoxia-sensitive tissues, such as the brain and heart (Irving et al, 1941;Scholander et al, 1942). However, blood oxygen supplementation to working muscle can occur during moderate bradycardias that are common during routine dives and breath-holds of diving animals (Guyton et al, 1995;Jobsis et al, 2001;Ponganis et al, 2008;Williams et al, 2011). In addition, the positive relationship between heart rate and flipper stroke rate in some diving mammals has led to the hypothesis that exercise and muscle workload modulate the dive response and increase heart rate during short duration dives (Davis and Williams, 2012).…”

Section: Introductionmentioning

confidence: 99%

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Flipper stroke rate and venous oxygen levels in free-ranging California sea lions

Tift

Hückstädt

McDonald

et al. 2017

Journal of Experimental Biology

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The depletion rate of the blood oxygen store, development of hypoxemia and dive capacity are dependent on the distribution and rate of blood oxygen delivery to tissues while diving. Although blood oxygen extraction by working muscle would increase the blood oxygen depletion rate in a swimming animal, there is little information on the relationship between muscle workload and blood oxygen depletion during dives. Therefore, we examined flipper stroke rate, a proxy of muscle workload, and posterior vena cava oxygen profiles in four adult female California sea lions (Zalophus californianus) during foraging trips at sea. Flipper stroke rate analysis revealed that sea lions minimized muscle metabolism with a stroke-glide strategy when diving, and exhibited prolonged glides during the descent of deeper dives (>100 m). During the descent phase of these deep dives, 55± 21% of descent was spent gliding, with the longest glides lasting over 160 s and covering a vertical distance of 340 m. Animals also consistently glided to the surface from 15 to 25 m depth during these deeper dives. Venous hemoglobin saturation (S O2 ) profiles were highly variable throughout dives, with values occasionally increasing during shallow dives. The relationship between S O2 and flipper stroke rate was weak during deeper dives, while this relationship was stronger during shallow dives. We conclude that (1) the depletion of oxygen in the posterior vena cava in deep-diving sea lions is not dependent on stroke effort, and (2) stroke-glide patterns during dives contribute to a reduction of muscle metabolic rate.

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“…Such plasticity in blood flow distribution has also been observed in diving emperor penguins (Williams et al, 2011). Max.…”

Section: Discussion Flipper Stroke Patternssupporting

confidence: 52%

Section: Introductionmentioning

confidence: 99%

Flipper stroke rate and venous oxygen levels in free-ranging California sea lions

Tift

Hückstädt

McDonald

et al. 2017

Journal of Experimental Biology

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“…The filoplumes we discovered adjacent to contour feathers may play a similarly important survival role. By signalling the occurrence and location of a displaced feather, filoplumes may be key to maintaining an impermeable exterior, as well as the smooth hydrodynamic shape that probably contributes to a low cost of diving in emperor penguins [35]. Finally, perhaps explaining earlier omissions, we find it a special irony that the most abundant feathers on the penguin, the plumules, are never seen under normal circumstances.…”

Section: Resultsmentioning

confidence: 64%

Hidden keys to survival: the type, density, pattern and functional role of emperor penguin body feathers

2015

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Antarctic penguins survive some of the harshest conditions on the planet. Emperor penguins breed on the sea ice where temperatures drop below 2408C and forage in 21.88C waters. Their ability to maintain 388C body temperature in these conditions is due in large part to their feathered coat. Penguins have been reported to have the highest contour feather density of any bird, and both filoplumes and plumules (downy feathers) are reported absent in penguins. In studies modelling the heat transfer properties and the potential biomimetic applications of penguin plumage design, the insulative properties of penguin plumage have been attributed to the single afterfeather attached to contour feathers. This attribution of the afterfeather as the sole insulation component has been repeated in subsequent studies. Our results demonstrate the presence of both plumules and filoplumes in the penguin body plumage. The downy plumules are four times denser than afterfeathers and play a key, previously overlooked role in penguin survival. Our study also does not support the report that emperor penguins have the highest contour feather density.

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“…It should also be noted that we have assumed that stroke rate is an adequate index of muscle workload. It is possible that stroke thrust and amplitude may vary with individual strokes, and also contribute to muscle workload (Williams et al, 2011). These parameters await further investigation.…”

Section: Stroke Ratementioning

confidence: 99%

Stroke rates and diving air volumes of emperor penguins: implications for dive performance

Sato

Shiomi

Marshall

et al. 2011

Journal of Experimental Biology

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SUMMARYEmperor penguins (Aptenodytes forsteri), both at sea and at an experimental dive hole, often have minimal surface periods even after performance of dives far beyond their measured 5.6min aerobic dive limit (ADL: dive duration associated with the onset of post-dive blood lactate accumulation). Accelerometer-based data loggers were attached to emperor penguins diving in these two different situations to further evaluate the capacity of these birds to perform such dives without any apparent prolonged recovery periods. Minimum surface intervals for dives as long as 10min were less than 1min at both sites. Stroke rates for dives at sea were significantly greater than those for dives at the isolated dive hole. Calculated diving air volumes at sea were variable, increased with maximum depth of dive to a depth of 250m, and decreased for deeper dives. It is hypothesized that lower air volumes for the deepest dives are the result of exhalation of air underwater. Mean maximal air volumes for deep dives at sea were approximately 83% greater than those during shallow (<50m) dives. We conclude that (a) dives beyond the 5.6min ADL do not always require prolongation of surface intervals in emperor penguins, (b) stroke rate at sea is greater than at the isolated dive hole and, therefore, a reduction in muscle stroke rate does not extend the duration of aerobic metabolism during dives at sea, and (c) a larger diving air volume facilitates performance of deep dives by increasing the total body O 2 store to 68ml O 2 kg -1 . Although increased O 2 storage and cardiovascular adjustments presumably optimize aerobic metabolism during dives, enhanced anaerobic capacity and hypoxemic tolerance are also essential for longer dives. This was exemplified by a 27.6min dive, after which the bird required 6min before it stood up from a prone position, another 20min before it began to walk, and 8.4h before it dived again.

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What triggers the aerobic dive limit? Patterns of muscle oxygen depletion during dives of emperor penguins

Cited by 54 publications

References 68 publications

Flipper stroke rate and venous oxygen levels in free-ranging California sea lions

Flipper stroke rate and venous oxygen levels in free-ranging California sea lions

Hidden keys to survival: the type, density, pattern and functional role of emperor penguin body feathers

Stroke rates and diving air volumes of emperor penguins: implications for dive performance

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