Deep-diving sea lions exhibit extreme bradycardia in long-duration dives

McDonald, Birgitte I.; Ponganis, Paul J.

doi:10.1242/jeb.098558

Cited by 53 publications

(72 citation statements)

References 43 publications

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“…In some cases, ΔS O2 appeared to be affected by stroke rate patterns as would be expected during exercise and consistent with recent suggestions that heart rate (and presumably some muscle blood flow) is modulated by exercise (Davis and Williams, 2012;Williams et al, 2015). During shallow dives, California sea lions exhibit higher heart rates than those seen during deep dives (McDonald and Ponganis, 2014). These higher heart rates are likely associated with increased blood flow to muscle, and could account for the relationship between flipper stroke rates and venous blood oxygen depletion during shallow dives.…”

Section: Discussion Flipper Stroke Patternssupporting

confidence: 86%

“…The maintenance of high arterial hemoglobin saturation (McDonald and Ponganis, 2012), despite the posterior vena caval S O2 decreasing to extremely low values during deep dives, suggests the presence of a central venous oxygen pool that is slowly depleted during the severe bradycardias seen in deep dive (McDonald and Ponganis, 2014). Otherwise, in the presence of lung collapse and lack of gas exchange, arterial hemoglobin saturation should reflect the low venous values observed in the posterior vena cava.…”

Section: Discussion Flipper Stroke Patternsmentioning

confidence: 99%

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

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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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Section: Discussion Flipper Stroke Patternssupporting

confidence: 86%

Section: Discussion Flipper Stroke Patternsmentioning

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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“…For dolphins and the three pinniped species noted above, ectopic heart beats were most apparent during ascents from the deepest foraging dives 28,29 (Fig. 3c).…”

Section: Discussionmentioning

confidence: 82%

Exercise at depth alters bradycardia and incidence of cardiac anomalies in deep-diving marine mammals

et al. 2015

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Unlike their terrestrial ancestors, marine mammals routinely confront extreme physiological and physical challenges while breath-holding and pursuing prey at depth. To determine how cetaceans and pinnipeds accomplish deep-sea chases, we deployed animal-borne instruments that recorded high-resolution electrocardiograms, behaviour and flipper accelerations of bottlenose dolphins (Tursiops truncatus) and Weddell seals (Leptonychotes weddellii) diving from the surface to 4200 m. Here we report that both exercise and depth alter the bradycardia associated with the dive response, with the greatest impacts at depths inducing lung collapse. Unexpectedly, cardiac arrhythmias occurred in 473% of deep, aerobic dives, which we attribute to the interplay between sympathetic and parasympathetic drivers for exercise and diving, respectively. Such marked cardiac variability alters the common view of a stereotypic 'dive reflex' in diving mammals. It also suggests the persistence of ancestral terrestrial traits in cardiac function that may help explain the unique sensitivity of some deep-diving marine mammals to anthropogenic disturbances.

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“…It has long been known that the magnitude of the dive response varies, depending on the nature of a given dive or breath hold (Andrews et al, 1997;Elsner et al, 1966Elsner et al, , 1989Elsner et al, , 1964Irving et al, 1941;Jobsis et al, 2001;Ponganis et al, 1997;Thompson and Fedak, 1993). The most severe bradycardias (see Glossary) and intense vasoconstriction typically occur during forced submersions; however, extremely low heart rates can also occur during some dives and segments of dives in the wild (Andrews et al, 1997;McDonald and Ponganis, 2014;Scholander, 1940;Scholander et al, 1942;Thompson and Fedak, 1993).…”

Section: Neuroregulation Of the Dive Responsementioning

confidence: 99%

Heart rate regulation in diving sea lions: the vagus nerve rules

Ponganis

McDonald

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et al. 2017

Journal of Experimental Biology

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Recent publications have emphasized the potential generation of morbid cardiac arrhythmias secondary to autonomic conflict in diving marine mammals. Such conflict, as typified by cardiovascular responses to cold water immersion in humans, has been proposed to result from exercise-related activation of cardiac sympathetic fibers to increase heart rate, combined with depth-related changes in parasympathetic tone to decrease heart rate. After reviewing the marine mammal literature and evaluating heart rate profiles of diving California sea lions (Zalophus californianus), we present an alternative interpretation of heart rate regulation that de-emphasizes the concept of autonomic conflict and the risk of morbid arrhythmias in marine mammals. We hypothesize that: (1) both the sympathetic cardiac accelerator fibers and the peripheral sympathetic vasomotor fibers are activated during dives even without exercise, and their activities are elevated at the lowest heart rates in a dive when vasoconstriction is maximal, (2) in diving animals, parasympathetic cardiac tone via the vagus nerve dominates over sympathetic cardiac tone during all phases of the dive, thus producing the bradycardia, (3) adjustment in vagal activity, which may be affected by many inputs, including exercise, is the primary regulator of heart rate and heart rate fluctuations during diving, and (4) heart beat fluctuations (benign arrhythmias) are common in marine mammals. Consistent with the literature and with these hypotheses, we believe that the generation of morbid arrhythmias because of exercise or stress during dives is unlikely in marine mammals.

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Deep-diving sea lions exhibit extreme bradycardia in long-duration dives

Cited by 53 publications

References 43 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

Exercise at depth alters bradycardia and incidence of cardiac anomalies in deep-diving marine mammals

Heart rate regulation in diving sea lions: the vagus nerve rules

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