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Drivers of the dive response in pinnipeds; apnea, submergence or temperature? [RESEARCH ARTICLE]

Jeppe Kaczmarek, Colleen Reichmuth, Birgitte I. McDonald, Jakob H. Kristensen, Josefin Larson, Fredrik Johansson, Jenna L. Sullivan, and Peter T. Madsen

Long and deep dives in marine mammals are enabled by high mass-specific oxygen stores and the dive response, which reduces oxygen consumption in concert with increased peripheral vasoconstriction and a lowered heart rate during dives. Diving heart rates of pinnipeds are highly variable and modulated by many factors, such as breath holding (apnea), pressure, swimming activity, temperature and even cognitive control. However, the individual effects of these factors on diving heart rate are poorly understood because of the difficulty of parsing their relative contributions in diving pinnipeds. Here, we examined the effects of apnea and external sensory inputs as autonomic drivers of bradycardia. Specifically, we hypothesized that (1) water stimulation of facial receptors would – as is the case for terrestrial mammals – enhance the dive response, (2) increasing the facial area stimulated would lead to a more intense bradycardia, and (3) cold water would elicit a more pronounced bradycardia than warm water. Three harbor seals (Phoca vitulina) and a California sea lion (Zalophus californianus) were trained to breath hold in air and with their heads submerged in a basin with variable water level and temperature. We show that bradycardia occurs during apnea without immersion. We also demonstrate that bradycardia is strengthened by both increasing the area of facial submersion and colder water. Thus, we conclude that the initiation of the dive response in pinnipeds is more strongly related to breath holding than in terrestrial mammals, but the degree of the dive response is potentiated autonomically via stimulation of facial mechano- and thermo-receptors upon submergence.

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