First published online May 24, 2005
Journal of Experimental Biology 208, 2071-2082 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01575
Using ultrasound to understand vascular and mantle contributions to venous return in the cephalopod Sepia officinalis L.
Alison J. King1,*,
Stephen M. Henderson4,
Matthias H. Schmidt2,
Alison G. Cole1,
and
Shelley A. Adamo3
1 Department of Biology, Dalhousie University, Halifax, NS,
Canada
2 Department of Radiology, Dalhousie University, Halifax, NS,
Canada
3 Department of Psychology, Dalhousie University, Halifax, NS,
Canada
4 Scripps Institution of Oceanography, La Jolla, CA 92093-0209,
USA

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Fig. 1. The circulatory system of S. officinalis viewed from below
(modified from Schipp, 1987b ).
White rectangles indicate planes along which ultrasound images were taken. See
Materials and methods for organs transected in each numbered plane. Stippled
vessels carry deoxygenated blood; dark vessels carry oxygenated blood. ABV,
afferent branchial vessel; AMV, anterior mantle vein; AU, auricle; AVC,
anterior vena cava (Point A, near the opening of the mantle; Point B, near the
opening of the anus); BH, branchial heart; BP, branch point; CA, cephalic
aorta; EBV, efferent branchial vessel; LVC, lateral venae cavae; PMV,
posterior mantle vein; PAO, posterior aorta; V, ventricle.
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Fig. 2. Schematic diagram of the experimental set-up. Water was fed into the inner
compartment of the experimental tank through perforated airline tubing. It
then passed to the outer compartment through many small holes and was drained
by a siphon. The cuttlefish (black) was placed in the inner compartment.
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Fig. 3. Ultrasound images illustrating the spatial relationships between organs in
a non-dissected cuttlefish. The dorsal mantle is always at the top of the
image, and the ventral mantle is always at the bottom. Non-cardiovascular
organs are abbreviated with lower case letters. (A) Transverse section through
the anterior mantle. (B) Midsagittal section showing organs from planes 1 and
2 of Fig. 1 (see supplementary
material, Movie 1). The head is towards the right. (C) Transverse section
through the branch point and the efferent branchial vessels (plane 3,
Fig. 1; also see supplementary
material, Movie 2). (D) An oblique transverse section through the ventricle.
Organs visible on the right are posterior to those on the left. This roughly
corresponds to plane 4 in Fig.
1. Nidamental glands (ng) are present only in females. AU,
auricle; AVC, anterior vena cava; BP, branch point; cf, collar flap; dg,
digestive gland; EBV, efferent branchial vessel; f, funnel; int, shared course
of the intestine and ink sac duct; LVC, lateral venae cavae; m, mantle; V,
ventricle. All scale bars are 2 cm.
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Fig. 4. Phase shift between the maximum contraction of the ventricle (arbitrarily
set at 0°) and the branch point (open circles; BP in
Fig. 1), the lateral venae
cavae (grey circles; LVC in Fig.
1), the branchial hearts (black circles; BH in
Fig. 1) and the efferent
branchial vessels (hatched circles, EBV in
Fig. 1). Time proceeds
clockwise. Each concentric circumference shows the averaged data for one
cuttlefish. NS indicates averages calculated from raw data that were not
significantly similar (significance only determined if there were more than
two data points. There were never more than four data points). Because data on
the efferent branchial vessel and ventricle were not collected simultaneously,
contraction phase of the efferent branchial vessel was calculated from its
average phase shift from the average phase shift of the branch point. We
obtained no data on the branchial heart for the cuttlefish of innermost
circumference.
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Fig. 5. (A) Schematic representation of the valve when open. Blood travels from the
anterior vena cava (AVC) into the lateral venae cavae (LVC). When blood
pressure rises in the LVC relative to the AVC, the valve closes. (B) Blue
tracing medium in the AVC (circled). (C) Once tracing medium was pushed from
the AVC (circled) into the branch point, it could not be pushed back into the
AVC. Scale bar, 1 cm. (D) Close to the lateral wall, the valve spanned the
whole vessel (x6 magnification; scale bar, 0.5 mm). (E) Mid-sagittally a
natural split occurred in the valve tissue. We verified that it was not an
artifact through analysis of successive serial sections. The distal end of the
larger portion of the valve tissue was reinforced by a polysaccharide-rich
thickening (x6 magnification; scale bar, 0.5 mm). (F) The muscular,
small side of the valve, indicated by a broken box in E. Muscle cells stained
red (x60 magnification; scale bar, 50 µm). AVC, anterior vena cava;
BP, branch point; LVC, lateral venae cavae; PAV, posterior azygos vein.
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Fig. 6. Phase shifts between the contraction cycle of the mantle and the
contraction cycle of Point A on the anterior vena cava (AVC). Full expansion
of the mantle is arbitrarily set at 0° and time proceeds clockwise. The
heavy black line starts at the full contraction of Point A (AVC) and ends at
the full expansion of Point A. The heavy grey line starts at full mantle
contraction and ends at full mantle expansion. Each concentric circumference
represents the averaged data of a different cuttlefish.
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Fig. 7. The phase shift between the mantle and the anterior vena cava (AVC) plotted
against the ventilation rate: heart rate ratio.
Fig. 6 shows the variation in
the phase shift between mantle and AVC contractions between animals. This
variation is largely explained by how many times the mantle contracts per
heart contraction (linear regression: r2=0.98,
P=0.0082, N=4). Each symbol represents averaged data from
one cuttlefish.
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© The Company of Biologists Ltd 2005