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

Abstract

SUMMARYFin whales have an incompliant aorta, which, we hypothesize, represents an adaptation to large, depth-induced variations in arterial transmural pressures. We hypothesize these variations arise from a limited ability of tissues to respond to rapid changes in ambient ocean pressures during a dive. We tested this hypothesis by measuring arterial mechanics experimentally and modelling arterial transmural pressures mathematically. The mechanical properties of mammalian arteries reflect the physiological loads they experience, so we examined a wide range of fin whale arteries. All arteries had abundant adventitial collagen that was usually recruited at very low stretches and inflation pressures (2-3kPa), making arterial diameter largely independent of transmural pressure. Arteries withstood significant negative transmural pressures (−7 to −50kPa) before collapsing. Collapse was resisted by recruitment of adventitial collagen at very low stretches. These findings are compatible with the hypothesis of depth-induced variation of arterial transmural pressure. Because transmural pressures depend on thoracic pressures, we modelled the thorax of a diving fin whale to assess the likelihood of significant variation in transmural pressures. The model predicted that deformation of the thorax body wall and diaphragm could not always equalize thoracic and ambient pressures because of asymmetrical conditions on dive descent and ascent. Redistribution of blood could partially compensate for asymmetrical conditions, but inertial and viscoelastic lag necessarily limits tissue response rates. Without pressure equilibrium, particularly when ambient pressures change rapidly, internal pressure gradients will develop and expose arteries to transient pressure fluctuations, but with minimal hemodynamic consequence due to their low compliance.

Morphological structure of the aortic wall in three Delphinid species with shallow or intermediate diving habits: Evidence for diving adaptation

“…The cardiovascular adaptations of the marine mammals allow for the diving habits. Among these adaptations, an expansive ascending aorta or an expansive aortic arch and a non-compliant or low compliant descending aorta have been described (Drabek, 1975;Lille, Piscitelli, Volg, Gosline, & Shadwick, 2013;Melnikov, 1997;Shadwick & Gosline, 1994, 1995. These characteristics are considered the aortic adaptations of some marine mammals for diving.…”

Under pressure: biomechanical limitations of developing pneumatocysts in the bull kelp (Nereocystis luetkeana, Phaeophyceae)

“…Other biological materials are known to similarly specialize in either compression (mammalian bone, Reilly and Burstein , cetacean heart valves, Lillie et al. ) or tension (mussel byssus, Bell and Gosline , aquatic plants, Etnier and Villani ). Future work should examine the histological differences that may exist between Nereocystis pneumatocyst tissue, which resists compression, and Nereocystis stipe tissue, which is known to resist tension (Johnson and Koehl , Denny et al.…”

Using morphology to infer physiology: case studies on rorqual whales (Balaenopteridae)

“…subsequent study byLillie et al 2013 found that, with the exception of a few arteries right off the arch 371 that had the same high distensibility as the arch, all the other arteries examined from a fin whale 372…”

“…The model described by Lillie et al 2013 predicted that transient differences between thoracic and 466 ambient pressure will develop during the descent and ascent portion of a dive, and that the gradients 467 can eventually be ameliorated by a shift in blood volume, possibly into the thoracic retia or aortic arch. If 468 these predictions prove accurate, the arteries must experience a wider range of transmural pressures 469 than normally associated with mammalian circulation, making the absence of compliance in the 470 peripheral arteries a possible adaptation to deal with these pressure effects.…”

“…314of arterial compliance to the aortic arch(Shadwick and Gosline 1994b), and the presence of extensive 315 vascular retia(Harrison and Tomlinson 1956;Lillie et al 2013;Slijper 1979). 316317In terrestrial mammals, the aorta and the major branching arteries are compliant elastic conduits that 318 expand with blood during cardiac ejection (systole) and maintain flow by elastic recoil of the vessel walls 319 during cardiac filling (diastole).…”