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Changes in partial pressures of respiratory gases during submerged voluntary breath hold across odontocetes: is body mass important?

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Abstract

Odontocetes have an exceptional range in body mass spanning 103 kg across species. Because, size influences oxygen utilization and carbon dioxide production rates in mammals, this lineage likely displays an extraordinary variation in oxygen store management compared to other marine mammal groups. To examine this, we measured changes in the partial pressures of respiratory gases (\( P_{{{\text{O}}_{2} }} \), \( P_{{{\text{CO}}_{2} }} \)), pH, and lactate in the blood during voluntary, quiescent, submerged breath holds in Pacific white-sided dolphins (Lagenorhynchus obliquidens), bottlenose dolphins (Tursiops truncatus), and a killer whale (Orcinus orca) representing a mass range of 96–3,850 kg. These measurements provided an empirical determination of the effect of body size on the variability in blood biochemistry during breath hold and experimentally determined aerobic dive limits (ADL) within one taxonomic group (odontocetes). For the species in this study, maximum voluntary breath-hold duration was positively correlated with body mass, ranging from 3.5 min in white-sided dolphins to 13.3 min for the killer whale. Variation in breath-hold duration was associated with differences in the rate of change for \( P_{{{\text{O}}_{2} }} \) throughout breath hold; \( P_{{{\text{O}}_{2} }} \) decreased twice as fast for the two smaller species (−0.6 mmHg O2 min−1) compared to the largest species (−0.3 mmHg O2 min−1). In contrast, the rate of increase in \( P_{{{\text{CO}}_{2} }} \) during breath hold was similar across species. These results demonstrate that large body size in odontocetes facilitates increased aerobic breath-hold capacity as mediated by decreased mass-specific metabolic rates (rates of change in \( P_{{{\text{O}}_{2} }} \) served as a proxy for oxygen utilization). Indeed the experimentally determined 5 min ADL for bottlenose dolphins was surpassed by the 13.3 min maximum breath hold of the killer whale, which did not end in a rise in lactate. Rather, breath hold ended voluntarily as respiratory gases and pH fell within a narrow range for both large and small species, likely providing cues for ventilation.

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Acknowledgments

We thank the staff and animals at John G. Shedd Aquarium, Oregon Coast Aquarium and Free Willy Keiko Foundation, and Naval Ocean Systems Center; this work would not have been possible without them. We thank D.P. Noren for assistance with the Pacific white-sided dolphin study. This study was funded by: Office of Naval Research Marine Mammal Program award #N00014-00-1-0761 to T.M. Williams, Shedd Aquarium Aquatic Science Partnerships Program supported by Dr. Scholl Foundation awarded to T.M. Williams and S.R. Noren, Lerner-Gray Fund for Marine Research from American Museum of Natural History awarded to S.R Noren, and American Cetacean Society (Monterey Bay Chapter Grant) awarded to S.R. Noren. All materials and methods and all experiments comply with the current laws of the United States of America and were approved by the Chancellor’s Animal Research Committee of the University of California at Santa Cruz.

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Correspondence to S. R. Noren.

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Communicated by H.V. Carey.

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Noren, S.R., Williams, T.M., Ramirez, K. et al. Changes in partial pressures of respiratory gases during submerged voluntary breath hold across odontocetes: is body mass important?. J Comp Physiol B 182, 299–309 (2012). https://doi.org/10.1007/s00360-011-0612-0

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