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The marine mammal dive response is exercise modulated to maximize aerobic dive duration

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Abstract

When aquatically adapted mammals and birds swim submerged, they exhibit a dive response in which breathing ceases, heart rate slows, and blood flow to peripheral tissues and organs is reduced. The most intense dive response occurs during forced submersion which conserves blood oxygen for the brain and heart, thereby preventing asphyxiation. In free-diving animals, the dive response is less profound, and energy metabolism remains aerobic. However, even this relatively moderate bradycardia seems diametrically opposed to the normal cardiovascular response (i.e., tachycardia and peripheral vasodilation) during physical exertion. As a result, there has been a long-standing paradox regarding how aquatic mammals and birds exercise while submerged. We hypothesized based on cardiovascular modeling that heart rate must increase to ensure adequate oxygen delivery to active muscles. Here, we show that heart rate (HR) does indeed increase with flipper or fluke stroke frequency (SF) during voluntary, aerobic dives in Weddell seals (HR = 1.48SF − 8.87) and bottlenose dolphins (HR = 0.99SF + 2.46), respectively, two marine mammal species with different evolutionary lineages. These results support our hypothesis that marine mammals maintain aerobic muscle metabolism while swimming submerged by combining elements of both dive and exercise responses, with one or the other predominating depending on the level of exertion.

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Abbreviations

ECG:

Electrocardiogram

Hb:

Hemoglobin

HR:

Heart rate (min−1)

kPa:

Kilopascal

Mb:

Myoglobin

O2 :

Oxygen

ODBA:

Overall dynamic body acceleration

P 50 :

Oxygen partial pressure (mm Hg or kPa) at 50 % saturation

RMSD:

Root-mean-square difference

SF:

Flipper or fluke stroke frequency (min−1)

VHF:

Very high frequency

\( \dot{V}_{{{\text{O}}_{2} }} \) :

Rate of oxygen consumption (ml O2 min−1 kg−1)

\( \dot{V}_{{{\text{MO}}_{2} }} \) :

Multiple of resting skeletal muscle oxygen consumption

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Acknowledgments

We thank the following people for field assistance: W. Buitenkyk, G. Davis, I. Davis, T. Kendall, B. Richter, and D. Williams. Field and statistical assistance was provided by E. Farrell and L. Fuiman. Assistance with instrument development was provided by W. Hagey. This study was supported by Grants from the Office of Naval Research (N000140811273 to T.M. Williams) and National Science Foundation Polar Programs (OPP0739390 to R. Davis, OPP0739163 to T.M. Williams). We also thank P. Berry and the dolphin behavior team at EPCOT Center, Disney World for providing and training the dolphins in this study and for assisting in the research. All experimental procedures were conducted in accordance with the Institutional Animal Use and Care Committees at Texas A&M University, the University of California at Santa Cruz, and Disney EPCOT. This study was conducted under Marine Mammal Permit Nos. 984-1814-01 and 984-1587-00.

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Authors and Affiliations

  1. Department of Marine Biology, Texas A&M University, OCSB, 200 Seawolf Parkway, Galveston, TX, 77553, USA

    Randall W. Davis

  2. Center for Ocean Health, University of California, 100 Shaffer Road, Santa Cruz, CA, 95060, USA

    Terrie M. Williams

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  1. Randall W. Davis
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Correspondence to Randall W. Davis.

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Davis, R.W., Williams, T.M. The marine mammal dive response is exercise modulated to maximize aerobic dive duration. J Comp Physiol A 198, 583–591 (2012). https://doi.org/10.1007/s00359-012-0731-4

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  • DOI: https://doi.org/10.1007/s00359-012-0731-4

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