Abstract

Diving mammals have evolved a suite of physiological adaptations to manage respiratory gases during extended breath-hold dives. To test the hypothesis that offshore bottlenose dolphins have evolved physiological adaptations to improve their ability for extended deep dives and as protection for lung barotrauma, we investigated the lung function and respiratory physiology of four wild common bottlenose dolphins (Tursiops truncatus) near the island of Bermuda. We measured blood hematocrit (Hct, %), resting metabolic rate (RMR, l O2 ⋅ min-1), tidal volume (VT, l), respiratory frequency (fR, breaths ⋅ min-1), respiratory flow (l ⋅ min-1), and dynamic lung compliance (CL, l ⋅ cmH2O-1) in air and in water, and compared measurements with published results from coastal, shallow-diving dolphins. We found that offshore dolphins had greater Hct (56 ± 2%) compared to shallow-diving bottlenose dolphins (range: 30–49%), thus resulting in a greater O2 storage capacity and longer aerobic diving duration. Contrary to our hypothesis, the specific CL (sCL, 0.30 ± 0.12 cmH2O-1) was not different between populations. Neither the mass-specific RMR (3.0 ± 1.7 ml O2 ⋅ min-1 ⋅ kg-1) nor VT (23.0 ± 3.7 ml ⋅ kg-1) were different from coastal ecotype bottlenose dolphins, both in the wild and under managed care, suggesting that deep-diving dolphins do not have metabolic or respiratory adaptations that differ from the shallow-diving ecotypes. The lack of respiratory adaptations for deep diving further support the recently developed hypothesis that gas management in cetaceans is not entirely passive but governed by alteration in the ventilation-perfusion matching, which allows for selective gas exchange to protect against diving related problems such as decompression sickness.

Highlights

  • Marine mammals live a life of dual constraints: On one hand, they need to find and exploit prey in varying densities underwater, but on the other hand as air breathing animals they need to return to the surface to replenish oxygen consumption rate (O2) stores and remove CO2 produced by aerobic metabolism

  • Our aim was to compare these measurements with data from coastal ecotype bottlenose dolphins (Fahlman et al, 2018a) to test the hypothesis that deeper-diving offshore ecotype bottlenose dolphins have a lower mass-specific metabolic rate, a lower tidal volume (VT), and a greater CL as part of traits to improve the ability for extended deep dives and as protection against lung barotrauma

  • To further increase calculated aerobic dive limit (cADL), we previously proposed that the offshore ecotype have, in addition to reduced resting metabolic rate (RMR) and blood Hct, increased blood volume, muscle mass and muscle myoglobin as compared with the coastal ecotype (Pabst et al, 2016)

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Summary

Introduction

Marine mammals live a life of dual constraints: On one hand, they need to find and exploit prey in varying densities underwater, but on the other hand as air breathing animals they need to return to the surface to replenish O2 stores and remove CO2 produced by aerobic metabolism. Many marine mammals have evolved to lower energy consumption over the dive and to increase available O2 stores. Oxygen stores are typically expanded by having a greater proportion of blood relative to body mass, by increasing the amount of red blood cells per volume of blood (the hematocrit), and by increasing the amount of myoglobin (Ponganis, 2015). It has been proposed that deep divers have relatively larger muscle mass, large muscle fibers, and low mitochondrial volume (Kooyman and Ponganis, 1998; Pabst et al, 2016). A greater proportion of blood volume and muscle mass would enhance available O2, and the latter would help to reduce the overall rate of O2 consumption as the basal metabolic rate of muscle is lower than many other tissues (Pabst et al, 2016). It is suggested that the reduced lung volume minimizes gas exchange at depth and minimizes uptake of N2 and thereby the risk of diving-related problems such as decompression sickness or N2 narcosis (Scholander, 1940; Kooyman, 1973; Bostrom et al, 2008)

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