Vascularization of Air Sinuses and Fat Bodies in the Head of the Bottlenose Dolphin (Tursiops truncatus): Morphological Implications on Physiology

Abstract

Cetaceans have long been considered capable of limiting diving-induced nitrogen absorption and subsequent decompression sickness through a series of behavioral, anatomical, and physiological adaptations. Recent studies however suggest that in some situations these adaptive mechanisms might be overcome, resulting in lethal and sublethal injuries. Perhaps most relevant to this discussion is the finding of intravascular gas and fat emboli in mass-stranded beaked whales. Although the source of the gas emboli has as yet to been ascertained, preliminary findings suggest nitrogen is the primary component. Since nitrogen gas embolus formation in divers is linked to nitrogen saturation, it seems premature to dismiss similar pathogenic mechanisms in breath-hold diving cetaceans. Due to the various anatomical adaptations in cetacean lungs, the pulmonary system is thought of as an unlikely site of significant nitrogen absorption. The accessory sinus system on the ventral head of odontocete cetaceans contains a sizeable volume of air that is exposed to the changing hydrostatic pressures during a dive, and is intimately associated with vasculature potentially capable of absorbing nitrogen through its walls. The source of the fat emboli has also remained elusive. Most mammalian fat deposits are considered poorly vascularized and therefore unlikely sites of intravascular introduction of lipid, although cetacean blubber may not be as poorly vascularized as previously thought. We present new data on the vasculature of air sinuses and acoustic fat bodies in the head of bottlenose dolphins and compare it to published accounts. We show that the mandibular fat bodies and accessory sinus system are associated with extensive venous plexuses and suggest potential physiological and pathological implications.

A comparative analysis of marine mammal tracheas

“…Additionally, the contribution of peritracheal and endotracheal tissue properties (e.g. engorgement of endotracheal venous plexus) was not investigated (Cozzi et al, 2005;Costidis and Rommel, 2012). Thus, the tracheal compliance in live animals may prove to be different.…”

“…Simple morphological comparisons between shallow diving species of cetacean and deep diving cetaceans (beaked whales) may not be appropriate, as they have demonstrated vastly different dive behavior. In addition, other anatomical features of the trachea may affect compliance; for example, connective tissue or the endotracheal venous plexus, which may fill and displace the intra-tracheal air volume (Cozzi et al, 2005;Costidis and Rommel, 2012). It would make sense that associated tissues as well as engorgement would affect compliance in measurements taken in situ rather than in excised tracheas.…”

Cardiovascular design in fin whales: high-stiffness arteries protect against adverse pressure gradients at depth

“…Venous structures have received little attention in cetaceans (Costidis and Rommel, 2012), and there are currently insufficient data to determine the adequacy of their volume or compliance for regulation of thoracic pressure in a fin whale. The aortic arch for an 18m fin whale has ample volume, holding ~56l at 13kPa and increasing essentially linearly with pressure from near zero to ~120l at 22kPa (Shadwick and Gosline, 1994).…”

“…Therefore, if shifting blood volumes offers a useful method of adjusting thoracic pressures, there needs be a reservoir of adequate volume that can rapidly adjust with depth, either passively or actively. Several vascular reservoirs in diving mammals have been identified for possible volume replacement: the aortic arch (Shadwick and Gosline, 1994), the thoracic rete (Barnett et al, 1958;Mcfarland et al, 1979;Walmsley, 1938), the tracheal rete (Cozzi et al, 2005) and venous structures within the thorax or associated with air-containing structures (Costidis and Rommel, 2012;Cozzi et al, 2005;Falke et al, 2008;Ninomiya et al, 2005).…”

The physiological consequences of breath-hold diving in marine mammals; the Scholander legacy

“…The DCS model assumptions are based on data from widely different species, which may explain the elevated predictions for marine mammals. A recent study by Costidis and Rommel (2012) provides data on the vascular anatomy in bottlenose dolphins, suggesting that certain adipose tissue compartments may be highly vascularized. The ability to exchange gases in these compartments would vastly alter our understanding of how these species manage gases underwater, and provide interesting research challenges for the future.…”