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.

Ventilation and gas exchange before and after voluntary static surface breath-holds in clinically healthy bottlenose dolphins, Tursiops truncatus

“…The results from the current study show a large variation in V T , f R and end-expired gas content following breath-holds ranging from 34 to 292 s. Maximal and average dive durations in shallow-diving nearshore dolphins are within this range (Fahlman et al, 2018b;Wells et al, 2013), and this ecotype may therefore show similar variation following diving. In addition, the change in respiratory effort following longer breath-holds to reduce the duration of recovery resulted in a complicated relationship between V T , end-expired gas content and recovery duration.…”

“…Based on these results, it appears that bottlenose dolphins have considerable scope to further increase respiratory effort following a breath-hold. While it is difficult to extrapolate this to freely swimming and diving animals, bottlenose dolphins may be capable of much longer (Fahlman et al, 2018b) or more active breath-holds with similar recovery rates. However, this warrants further study if respiratory variables are to be used to assess field metabolic rate.…”

Deciphering function of the pulmonary arterial sphincters in loggerhead sea turtles (Caretta caretta)

“…The contraction would help to manage the ventilation/perfusion mismatch to minimize uptake of gases with low solubility (N 2 ), while permitting exchange of gases with higher solubility (O 2 and CO 2 ) (Farhi and Yokoyama, 1967;West, 1962). A similar mechanism has recently been suggested for marine mammals (Fahlman et al, 2018;García-Párraga et al, 2018). The undivided chelonian heart provides for intracardiac shunts, and it is well established that pulmonary blood flow is reduced during diving, causing R-L shunts, while pulmonary flow increases during intermittent ventilation, where a L-R shunt may dominate (Burggren, 1977;Shelton and Burggren, 1976;Wang et al, 1997Wang et al, , 2001).…”

“…ventilation-perfusion ratio in the lung, they may avoid DCS, while retaining the ability to manage pulmonary O 2 stores and CO 2 levels during dives (Fahlman et al, 2018;García-Párraga et al, 2018). Failure of this mechanism, caused by fisheries interaction, may explain the high incidence of GE during enforced submersion of turtles (Fahlman et al, 2017a;García-Párraga et al, 2014).…”

“…Consequently, to use the pulmonary O 2 stores, dives should be shallower than the depth where the faveoli collapse and gas exchange ceases. However, a recent hypothesis suggests that management of the ventilationperfusion ratio provides a mechanism to selectively exchange gases of different solubility (Fahlman et al, 2018;García-Párraga et al, 2018).…”