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Journal of Experimental Biology partnership with Dryad

Cardiovascular design in fin whales: high-stiffness arteries protect against adverse pressure gradients at depth
M. A. Lillie, M. A. Piscitelli, A. W. Vogl, J. M. Gosline, R. E. Shadwick

SUMMARY

Fin 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.

FOOTNOTES

  • AUTHOR CONTRIBUTIONS

    M.A.L., J.M.G. and R.E.S. were involved in the conception of the study and the design and execution of the mechanical tests. M.A.L., M.A.P. and A.W.V. were involved in the morphological studies. All authors were involved in the model development, interpretation of findings, and the writing of the manuscript.

  • COMPETING INTERESTS

    No competing interests declared.

  • FUNDING

    This work was supported by Discovery Grants from the Natural Sciences and Engineering Research Council to J.M.G. and to A.W.V., and by a Discovery Accelerator Grant from the Natural Sciences and Engineering Research Council to R.E.S.

  • LIST OF SYMBOLS AND ABBREVIATIONS
    d1d5
    thorax dimensions shown in Fig. 11B
    Ediaph
    modulus of diaphragm
    Ethor
    circumferential modulus of thorax
    Ethor,optimum
    circumferential modulus of thorax required to set Pthor=Pamb
    Eθ
    circumferential modulus of artery
    F
    circumferential load on artery in uniaxial tests
    Fdiaph
    net force acting on diaphragm
    Fmech
    mechanical force of ribs resisting compression of thorax cavity
    Fthor
    net force acting on thorax
    H, h
    artery wall thickness in the unloaded and loaded artery
    hdiaph
    diaphragm thickness
    ID
    inner diameter
    L, l
    length of segment in the unloaded and pressurized artery
    Ldiaph
    length of diaphragm
    Lthor
    length of thorax
    MAV
    minimum air volume
    OD
    outer diameter
    Pamb
    ambient ocean pressure
    Pcollapse
    negative transmural pressure required to collapse artery
    Pextrathor
    extravascular pressure outside the thorax
    Pthor
    extravascular pressure inside the thorax
    R
    logarithmic mean radius of artery
    r1/3thor
    thorax radius 1/3 of the way across the wall from the inside
    R1/3thor
    unloaded thorax radius 1/3 of the way across the wall from the inside
    ri, rmid, ro
    inner, midwall and outer radius of the pressurized artery
    Ri, Rmid, Ro
    inner, midwall and outer radius of the unloaded artery
    ri,thor, ro,thor
    inner and outer radius of thorax
    Ri,thor, Ro,thor
    inner and outer radius of the unloaded thorax
    TLC
    total lung capacity
    Vair
    volume of air in lungs
    Vthor
    total volume of thorax
    Vtissue
    volume of tissue in thorax excluding air
    w
    width of unloaded artery ring in uniaxial test
    εdiaph
    diaphragm strain
    εthor
    circumferential strain on thorax
    εθ
    circumferential strain on artery
    Embedded Image
    circumferential stretch of thorax where j represents ro, rmid, r1/3 or ri
    λθ, λz
    mean circumferential and axial stretches on artery
    ν
    Poisson's ratio
    σdiaph
    stress on diaphragm
    〈σthor
    circumferential stress on thorax
    σθ
    circumferential stress on artery
    ϕ
    diaphragm angle shown in Fig. 11B
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