Modeling Tissue and Blood Gas Kinetics in Coastal and Offshore Common Bottlenose Dolphins, Tursiops truncatus

Abstract

Bottlenose dolphins (Tursiops truncatus) are highly versatile breath-holding predators that have adapted to a wide range of foraging niches from rivers and coastal ecosystems to deep-water oceanic habitats. Considerable research has been done to understand how bottlenose dolphins manage O₂ during diving, but little information exists on other gases or how pressure affects gas exchange. Here we used a dynamic multi-compartment gas exchange model to estimate blood and tissue O₂, CO₂, and N₂ from high-resolution dive records of two different common bottlenose dolphin ecotypes inhabiting shallow (Sarasota Bay) and deep (Bermuda) habitats. The objective was to compare potential physiological strategies used by the two populations to manage shallow and deep diving life styles. We informed the model using species-specific parameters for blood hematocrit, resting metabolic rate, and lung compliance. The model suggested that the known O₂ stores were sufficient for Sarasota Bay dolphins to remain within the calculated aerobic dive limit (cADL), but insufficient for Bermuda dolphins that regularly exceeded their cADL. By adjusting the model to reflect the body composition of deep diving Bermuda dolphins, with elevated muscle mass, muscle myoglobin concentration and blood volume, the cADL increased beyond the longest dive duration, thus reflecting the necessary physiological and morphological changes to maintain their deep-diving life-style. The results indicate that cardiac output had to remain elevated during surface intervals for both ecotypes, and suggests that cardiac output has to remain elevated during shallow dives in-between deep dives to allow sufficient restoration of O₂ stores for Bermuda dolphins. Our integrated modeling approach contradicts predictions from simple models, emphasizing the complex nature of physiological interactions between circulation, lung compression, and gas exchange.

Keywords: blood gases; decompression sickness; diving physiology; gas exchange; hypoxia; marine mammals; modeling and simulations.

Figure 1

(A) Normalized volume (V_A, alveolar volume; V_D, dead space/tracheal volume) vs. structural pressure for alveolar and dead space compliances based on the estimate from Bostrom et al. (2008), or updated estimates from bottlenose dolphins (Fahlman et al., 2011, 2015). (B) Differences in pulmonary shunt with old and updated compliance values for the respiratory system in dolphins during a representative dive to 150 m for an animal with a body composition like the Bermuda dolphin (Fahlman et al., 2009). The average compliant alveoli and medium compliant trachea were used for the base model, and this model was used as a basis of comparison with all other simulations. Changes in end-dive mixed venous N₂, O₂, and CO₂ levels against (C) dive duration (sec) or (D) maximum dive depth (ATA) when comparing old and revised lung compliance values. The y-axis is the change in percent for [(old-new)/old ^* 100]. These changes reflect how the structural properties alter the shunt and ventilation-perfusion mismatch (Garcia Párraga et al., 2018).

Figure 2

Representative dive data from two bottlenose dolphins in Sarasota Bay, Florida (red line), and Bermuda (black line). Data are plotted on the same axes range to show the differences in diving capacity/behavior. Pressure in ATA where 1 ATA is at the surface and 2 ATA is at 10 m depth.

Figure 3

Dive depth vs. dive duration for (A) coastal Sarasota and (B) offshore Bermuda dolphins.

Figure 4

Estimated end-dive muscle PO₂ (kPa) vs. (A,C) dive duration or (B,D) maximum dive depth (ATA, 1 ATA = 98.07 kPa) in (A,B) Sarasota or (B,D) Bermuda dolphins.

Figure 5

(A,B) Estimated central circulation, muscle, brain, fat, arterial, and venous PO₂ (kPa) or (C,D) estimated shunt fraction, alveolar and tracheal volume for a long duration dive (depth in ATA, 1 ATA = 98.07 kPa) in (A,C) Sarasota and (B,D) Bermuda dolphin.