First published online August 25, 2003
Form and function of the bulbus arteriosus in yellowfin tuna (Thunnus albacares), bigeye tuna (Thunnus obesus) and blue marlin (Makaira nigricans): static properties
Marvin H. Braun1,*,
Richard W. Brill2,
John M. Gosline3 and
David R. Jones4
1 Department of Zoology, Cambridge University, Downing Street, Cambridge,
UK, CB2 3EJ
2 Cooperative Marine Education and Research Program, Virginia Institute of
Marine Science, PO Box 1208, Greate Rd, Gloucester Point, Virginia 23062,
USA
3 Department of Zoology, University of British Columbia, Vancouver, BC,
Canada, V6T 1Z4
4 Zoology Animal Care, 6199 South Campus Road, University of British
Columbia, Vancouver, BC, Canada, V6T 1W5
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Fig. 1. (A) The bulbus arteriosus from a yellowfin tuna. Scale bar, 5 cm.
(B) A yellowfin tuna bulbus opened to reveal longitudinal elements (l.e.).
Scale bar, 4 cm. (C) The bulbus of a blue marlin. Scale bar, 10 cm. (D) The
bulbus of a blue marlin cut open to reveal the l.e. Scale bar, 10 cm.
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Fig. 2. Yellowfin tuna fixed at ambient pressure. (A) Transverse section through
the longitudinal elements and media of the anterior bulbus. The elastin is
heavily stained and shows the circumferential alignment of the elastin fibres
(ef) in the media. The circumferential orientation of the elastin fibres is
changed to longitudinal within the longitudinal elements. Scale bar, 100
µm. (B) Transverse section of the ventral aorta less than 1 cm anterior
from the bulbus section in A. The wall of the ventral aorta is much thinner
than the wall of the bulbus and has elastin lamellae (el) separated by layers
of smooth muscle (sm). Collagen (co) is abundant within the adventitia. Scale
bar, 100 µm. (C) Longitudinal section of the posterior bulbus. Smooth
muscle occurs near the outer edge of the media, sandwiched between two layers
of longitudinal elastin fibres (lf). Scale bar, 100 µm. (D) Longitudinal
section of posterior bulbus. The smooth muscle layer shown in C is attached to
the pocket valve (V) separating the bulbus from the ventricle. Scale bar, 1
mm. Stained with Verhoeff's elastic stain.
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Fig. 3. Yellowfin tuna fixed at ambient pressure. All sections are transverse. (A)
Middle of the bulbus. A well-defined adventitia (a), outer media (om) and
inner media (im) are visible. In the dense outer media, elastin fibres are
arranged circumferentially. In the inner media, elastin fibres are arranged
longitudinally. The inner media contains the longitudinal elements (le). Scale
bar, 500 µm. (B) Posterior bulbus. The proportions of the adventitia, outer
media and inner media are changed. The outer media is half the thickness of
the same layer in the middle bulbus shown in A. The size and complexity of the
longitudinal elements have increased. Scale bar, 500 µm. (C) At the
transition between the inner media (IM) and outer media (OM), the
circumferential (cf) and longitudinal (lf) orientations of elastin fibres can
be seen. The long axes of the fibres in the outer media identify them as
circumferential while the small circles in the inner media show that the
fibres have been transected, indicating a longitudinal orientation. Scale bar,
50 µm. (D) Longitudinal elements (LE) with the same elastin fibre pattern
as the inner media. There are also radial elements (re) that attach the
longitudinal elements to the lumen wall. Scale bar, 50 µm. Stained with
Verhoeff's elastic stain.
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Fig. 4. Yellowfin tuna. All sections are transverse. (A) Electron micrograph of the
collagenous adventitia. The collagen fibres are not arranged in a single
direction. The majority of the fibres are arranged longitudinally (lf) but
there are also bundles of circumferential fibres (cf). Scale bar, 300 nm. (B)
Electron micrograph of the media. The long axes of the elastin fibrils are
aligned with the long axes of the smooth muscle cells, indicating a
circumferential arrangement. The smooth muscle cells possess a number of
plasmalemmal vesicles along the edge of the membrane (arrow). Scale bar, 1.45
µm. (C) Electron micrograph of smooth muscle within the bulbar media. The
smooth muscle cells are not always sparsely distributed within the elastin.
This section shows smooth muscle cells in close proximity. The smooth muscle
cells have plasmalemmal vesicles under the edge of the membrane (arrows).
Scale bar, 1.55 µm. (D) Electron micrograph of a longitudinal element (le).
The endothelial cells contain plasmalemmal vesicles underneath the membrane
(arrow) as well as larger, electron-dense vesicles scattered throughout the
cell (arrowheads). Scale bar, 1.55 µm. Stained with uranyl acetate and
lead.
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Fig. 5. Representative P-V loops from a yellowfin tuna bulbus arteriosus (b.a.), a
yellowfin tuna ventral aorta (v.a.), a blue marlin bulbus arteriosus, an
inside-out blue marlin bulbus arteriosus and a blue marlin ventral aorta. The
bar on the y-axis represents the physiological pressure range for
yellowfin tuna. Pressure range from Jones et al.
(1993 ).
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Fig. 6. Yellowfin tuna. Representative P-V loops from a parasitized dorsal aorta,
an unparasitized dorsal aorta and a bulbus arteriosus.
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Fig. 7. Yellowfin tuna (N=4). Mean P-V loops from fresh bulbi before and
after undergoing two treatments: a 10-5 mol l-1 solution
of nicardipine to inactivate the smooth muscle (s.m. blocked) and a high
temperature tissue bath to denature the collagen (heated). Values are means
± S.E.M.
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Fig. 8. Representative P-V loops from the bulbi of blue marlin. The bulbi have had
layers of the wall dissected away. The different treatments are: normal
(control); without l.e. (the longitudinal elements are removed) and without
l.e./inner (the longitudinal elements and inner media are removed).
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Fig. 9. Material properties of the adventitia (N=1) and outer media
(N=3) from yellowfin tuna bulbi. In vivo strains come from
Braun et al. (2001). (A) Stress-strain curves. (B) Modulus-strain curves.
Values are means ± S.E.M.
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Fig. 10. Material properties of segments from the bulbus (N=6) and ventral
aorta (N=3) of yellowfin tuna. In vivo strains come from
Braun et al. (2001). (A) Stress-strain curves of the anterior, middle, and
posterior portions of the bulbus. (B) Modulus-strain curves of the anterior,
middle and posterior portions of the bulbus. (C) Modulus-strain curves
comparing the ventral aorta to the anterior, middle and posterior portions of
the bulbus. Values are means ± S.E.M. The asterisk indicates
the modulus value for yellowfin tuna ventral aorta at mean physiological
pressure, as calculated by Shadwick
(1999) using vessel
inflations.
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Fig. 11. Material properties of different segments from the bulbus (N=4)
and ventral aorta (N=3) of blue marlin. (A) Stress-strain curves and
(B) modulus-strain curves of the anterior, middle and posterior portions of
the bulbus. (C) Modulus-strain curves comparing the ventral aorta to the
anterior, middle and posterior portions of the bulbus. Values are means
± S.E.M.
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Fig. 12. Material properties of the bulbi of yellowfin and bigeye tuna. (A)
Stress-strain curves. (B) Modulus-strain curves. The following rectangular
tissue samples were stretched using a micromanipulator: YF, yellowfin tuna;
BE, bigeye tuna; ML, segment of the middle layer; ILE, segment of longitudinal
element; OL, segment of the outer layer; circ., stretched circumferentially;
long., stretched longitudinally. The asterisk represents a tissue sample that
was stretched as a loop using the custom-built stretching machine.
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Fig. 13. Longitudinal sections from the bulbus arteriosus of yellowfin tuna. The
high pressure section was fixed at 14.7 kPa. The longitudinal elements (le)
are pushed to the side of the lumen (L) at high pressure. Scale bar, 1 mm.
Stained with Verhoeff's elastic stain.
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© The Company of Biologists Ltd 2003
