The extracranial venous system in the heads of beaked whales, with implications on diving physiology and pathogenesis

Abstract

Beaked whales are a poorly known but diverse group of whales that have received considerable attention due to strandings that have been temporally and spatially associated with naval sonar deployment. Postmortem studies on stranded carcasses have revealed lesions consistent with decompression sickness, including intravascular gas and fat emboli. These findings have been supported by analyses of intravascular gas emboli showing composition dominated by nitrogen gas. To increase our understanding of the pathophysiology of nitrogen bubble formation and intravascular embolization, we examined the gross and microscopic anatomy of the venous system in the head of beaked whales. Since the potential sources of intravascular fat and gas emboli were of greatest interest, focus was placed on the acoustic fat bodies and pneumatic accessory sinus system. Herein, we describe intimate arteriovenous associations with specialized adipose depots and air sinuses in beaked whales. These vascular structures comprise an extensive network of thin-walled vessels with a large surface area, which is likely to facilitate exchange of nitrogen gas and may, therefore, form anatomic regions that may be important in physiological management of diving gases. These structures may also be vulnerable to pathologic introduction of emboli into the vascular system. Expansive, thin-walled venous lakes are found within the pterygoid region, which suggest the potential for nitrogen exchange as well as for compensation of middle-ear pressures during descent on a dive. These findings warrant further research into the structure and function of this morphology as it relates to normal and pathologic physiology.

Function and evolution of specialized endogenous lipids in toothed whales

“…The acoustic tissues have significant macrovasculature (e.g. Costidis and Rommel, 2016), and it is hypothesized that these large vessels allow controlled flow of warmed blood to the acoustic fats to keep them in a constant phase for echolocation. Houser et al (2004) detected no metabolic activity in the acoustic tissues (a glucose analog was not taken up), which either means acoustic fat cells lack glucose transporters, or there is little direct exchange with the blood.…”

“…One missing piece of this puzzle is an understanding of the tissues from which the melon and mandibular fats are derived, which might help to elucidate how the synthesis and storage of wax esters first occurred -and these may have different origins. For example, Fraser and Purves (1960) proposed that the intra-mandibular fat body may be a highly modified form of bone marrow, whereas Costidis and Rommel (2016) suggested that the extra-mandibular fat body may be modified blubber. This is an interesting question given that the suites of lipids present in all acoustic depots within an individual are very similar.…”

Microvascular characteristics of the acoustic fats: Novel data suggesting taxonomic differences between deep and shallow‐diving odontocetes

“…However, it should be noted that these larger vessels show distinct heterogeneity in their distributions within the acoustic fats. In beaked whales for example, the extensive venous plexus in the IMFB is limited to the periphery of the tissue, with much reduced vascularity in the center (through which sound likely passes to the ears; Costidis & Rommel, ). We sampled this center region for our study and show that this area can differ by twofold to threefold in the density of small vessels.…”

“…We know that the acoustic tissues have the potential for increased blood flow. This is based on evidence from the arterial and venous anatomy of the jaw fats of beaked whales and bottlenose dolphins (Costidis & Rommel, 2012, 2016a, 2016bHouser et al, 2004). Specifically, the IMFB has a higher number of large vessels compared to the EMFB.…”

“…Specifically, the density of veins increases in the IMFB compared to the melon and EMFB (Costidis & Rommel, ). Deep‐diving beaked whales also have discrete networks of veins and arteries closely associated with the mandibular fats, further providing anatomical evidence that these tissues in cetaceans have the potential to undergo perfusion while diving (Costidis & Rommel, ). The close association between the blood vessels and adipose could result in an increased level of absorbed N 2 into the fat depots (especially given their high nitrogen solubility; see below), potentially causing damage in the tissue.…”