Dynamics of blood circulation during diving in the bottlenose dolphin (Tursiops truncatus). The role of the retia mirabilia

Abstract

The retia mirabilia are vascular nets composed of small vessels dispersed among numerous veins, allowing blood storage, regulation of flow and pressure damping effects. Here, we investigated their potential role during the diving phase of the bottlenose dolphin (Tursiops truncatus). To this effect, the whole vertebral retia mirabilia of a series of dolphins were removed during post-mortem analysis and examined to assess vessel diameters, and estimate vascular volume and flow rate. We formulated a new hemodynamic model to help clarify vascular dynamics throughout the diving phase, based on the total blood volume of a bottlenose dolphin, and using data available about the perfusion of the main organs and body systems. We computed the minimum blood perfusion necessary to the internal organs, and the stroke volume and cardiac output during the surface state. We then simulated breath-holding conditions and perfusion of the internal organs under the diving-induced bradycardia and reduction of stroke volume and cardiac output, using 10 beats min −1 as the limit for the heart rate for an extended dive of over 3 min. Within these simulated conditions, the retia mirabilia play a vital role as reservoirs of oxygenated blood that permit functional performances and survival of the heart and brain. Our theoretical model, based on the actual blood capacity of the retia mirabilia and available data on organ perfusion, considers the dynamic trend of vasoconstriction during the diving phase and may represent a baseline for future studies on the diving physiology of dolphins and especially for the blood supply to their brain.

Comparative morphology of the spinal cord and associated vasculature in shallow versus deep diving cetaceans

“…While this study has provided new quantitative data on the contents of the vertebral canal, many questions remain about the variable functions of the specialized vasculature therein. Over the centuries, the cetacean retial systems have been hypothesized to perform a variety of functions, including maintaining adequate cerebral blood flow, maintaining arterial blood pressure, changing the composition of arterial blood, maintaining the temperature of the central nervous system, facilitating thoracic collapse, filtering emboli, and providing dampening of pressure pulses of the cerebral blood supply (Tyson, 1680; Hunter, 1787; Owen, 1868; Murie, 1874; Cunningham, 1877; Wilson, 1879; MacKay, 1886; Ommanney, 1932; Slijper, 1936; Nakajima, 1961; Nagel et al, 1968; Hui, 1975; Reidenberg & Laitman, 2015; Bonato et al, 2019).…”

“…These results further suggest that deep diving marine mammals maintain perfusion of the brain during a dive. Because of the derived vascular morphology of cetaceans, the blood supply to the CNS, which lies within the vertebral canal, can be quantitatively assessed (e.g., Bonato et al, 2019).…”

“…To compare the relative size of vascular structures and spinal cord, the scaling relationship between these morphologic features and TBM were assessed across shallow and deep divers. The vascular structures associated with the CNS within the cetacean vertebral canal have been described morphologically and histologically in a small subset of species, including T. truncatus , M. monoceros , and D. leucas (Bonato et al, 2019; Vogl & Fisher, 1981; Vogl & Fisher, 1982). These studies have demonstrated that the retial tissue within the vertebral canal contains both the arterial vessels of the epidural rete and closely apposed veins, which receive blood from the dorsal body, spinal cord, and brain (e.g., Costidis, 2012).…”

“…The small veins within the epidural rete drain into the large caliber internal vertebral veins that lie on the ventral floor of the vertebral canal (personal observation). Currently, only one study, which examined T. truncatus , has provided a quantitative description of the epidural rete (Bonato et al, 2019). Bonato et al (2019) demonstrated the value of investigating these retial structures and their modeling suggested the epidural rete plays a critical role as a reservoir of oxygenated blood to the brain during a dive.…”

“…Currently, only one study, which examined T. truncatus , has provided a quantitative description of the epidural rete (Bonato et al, 2019). Bonato et al (2019) demonstrated the value of investigating these retial structures and their modeling suggested the epidural rete plays a critical role as a reservoir of oxygenated blood to the brain during a dive. Because of the larger mass‐specific blood volumes of deep divers, we predicted that the volume of these vascular structures would scale with positive allometry to display a positive allometric relationship with TBM across the shallow and deep divers investigated.…”