First published online July 20, 2007
Journal of Experimental Biology 210, 2627-2636 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.001644
Hemodynamics in the leech: blood flow in two hearts switching between two constriction patterns
Angela Wenning1,* and
Eric P. Meyer2
1 Department of Biology, Emory University, 1510 Clifton Road, Atlanta, GA
30322, USA
2 Institute of Zoology, University of Zürich, CH-8057 Zürich,
Switzerland
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Fig. 1. Scanning electron micrograph in a corrosion cast to show the heart, its two
afferent vessels, the latero-lateral (llv) and the larger latero-dorsal (ldv)
vessels, and the efferent latero-abdominal vessel (lav, inset). The afferent
vessels receive blood from the capillaries of the integument and body wall
musculature and are contractile up to their first bifurcation. Inset: removing
the capillaries (circle) reveals the latero-abdominal sphincter (arrowhead)
and the bifurcation of the efferent latero-abdominal vessel. Just anterior is
the heart sphincter of the next anterior heart segment (arrow). Due to the
pressure necessary for the resin injection (see text), the valves between the
side vessels and the heart (asterisks) are closed, as indicated by the
constriction between the two vessels. Some capillary beds were trimmed for
viewing purposes. Right body side, anterior to the top. Scale bars, 500
µm.
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Fig. 2. Assessment of total vessel capacity in corrosion casts (A,B) and dissected
animals (C,D). (A) Scanning electron micrograph of a transverse section
through a corrosion cast near the segmental border of segments 4 and 5 to show
the different vascular beds used to assess total vessel capacity: hearts;
afferent latero-dorsal vessels (asterisks); ventral vessel (1; with the
imprint of the connectives between the segmental ganglia); dorsal vessel (2);
capillary beds of the integument and the muscular envelope and capillary beds
of the inner organs (polygons). Note the small-caliber capillaries of the
integument and the somewhat larger capillaries of the adjacent layer in the
body wall musculature. Scale bar, 1 mm. (B) Blood vessel capacity was assessed
by dissecting and weighing the vascular beds of completely filled corrosion
casts. The graph shows the average of two casts. About 60% of the total blood
volume is stored in the capillary beds of the inner organs and the body wall
and its musculature. (C) Segment length and the end-diastolic diameter of
individual heart segments vary along the body axis. Segment length was
measured in eight intact leeches (grey squares). The diameter of individual
heart segments (blue triangles) and of the dorsal vessel in segment 10 (blue
filled circle) were measured in one cast. The end-diastolic diameters of the
hearts (red diamonds; number of measurements in italics), the afferent vessels
(green circles; ldv, latero-dorsal vessel; llv, latero-lateral vessel), the
latero-abdominal vessel (purple circle, lav) as well as the diameter of the
dorsal vessel (grey circle) were measured in freshly dissected leeches. Values
are plotted as a percentage of segment 10 (means ± s.d.). Absolute
values for segment 10 are given on the graph. (D) Using segment length and the
end-diastolic diameter, the end-diastolic volume was calculated for each heart
segment assuming a straight cylinder. All data from adult leeches.
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Fig. 3. Hemodynamic properties of the cardiac cycle (bar) in one heart segment to
show the timing of filling and emptying (example: heart segment 10). The
optical signal (black line) reflects the rhythmic filling (downward
deflection) and emptying (upward deflection) of the heart segment and yields
the information for the start of diastole (=10% filled), maximal diastole
(trough), the attainment of systole (`systole'; see Materials and methods for
definition) and the end of systole (=90% empty). Phase relations were based on
systole set at 0% phase. The period of one cardiac cycle was normalized to
100% phase (4.7±0.7 s in juvenile leeches). Systole of the afferent
vessels and the closure of the efferent latero-abdominal sphincter occurred at
the same time, just before maximal heart diastole (horizontal dotted
bars).
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Fig. 4. Filling of the hearts by segmental afferent vessels. (A) Scanning electron
micrograph of heart segments 15 and 16 in a corrosion cast in the intestinal
region. Left and right latero-dorsal vessels fuse (fusion area; small
asterisk) above the dorsal intestinal vessel (1) and form the latero-dorsal
arches (asterisks). The dotted line follows the left latero-dorsal arch of
segment 15 from its fusion point with the right arch to its valve at the
heart. In comparison, the latero-lateral vessel (llv) is smaller and shorter.
Its insertion point into the hearts is seen in two locations where the vessel
broke away (arrows). Note the ventral vessel (2) with the enlargement for the
ganglion of segment 15. Most capillary beds (integument, muscles, testes,
nephridia) were removed. Scale bar, 1 mm. (B) Optical recordings from the
latero-dorsal arch and the heart in the left hemisegment 15 (synchronous
mode). In this preparation, the latero-dorsal arch constricted before the
heart with an average phase difference of –23±3% (14 consecutive
beats). (C) A single cardiac cycle (shaded area in B) is enlarged and shows
the time points of the consecutive images of D. (D) Ventral aspect of segments
12–15 in the same animal as in B showing both hearts (arrows) and the
latero-dorsal arches (asterisks). Analysis windows were drawn around the left
heart of segment 15 and the latero-dorsal arch for optical recordings
(rectangle in a). Consecutive images (a–d) show the timing of the
constrictions of the latero-dorsal arch (dots) and the heart for the cardiac
cycle enlarged in C. (a) Latero-dorsal arch filled, heart partially filled;
(b) constriction of the latero-dorsal arch (no dots) fills the heart to
maximal diastole; (c) heart in systole; latero-dorsal arch fills; (d) heart
empty; latero-dorsal arch filled. Optical recordings are from intact juvenile
leeches. Anterior is to the top.
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Fig. 5. (A) Optical recordings from both hearts (black) in segment 11 and from the
latero-abdominal vessels (blue) and sphincters (red). The latero-abdominal
sphincters close briefly just before maximal diastole (asterisks), causing a
simultaneous interruption of flow in the vessels. (B) Position of the analysis
windows around the hearts and the latero-abdominal sphincter and vessel.
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Fig. 6. Phase diagram to illustrate the intersegmental and side-to-side
coordination of systole (vertical bars) in heart segments 3–18 for the
peristaltic (magenta) and the synchronous (blue) modes. Data are duplicated
and shifted by 100% to illustrate the side-to-side coordination over two
heartbeat cycles [values for systole from Wenning et al.
(Wenning et al., 2004a )].
Complete cardiac cycles (bars) are shown for segments 3, 6, 10 and 16
(labeling as in Fig. 3). Within
the period of one heartbeat cycle, the heart segments on both sides completed
their individual cardiac cycles. Starting with a nearly simultaneous systole
in segments 17–15 (set to 0% phase) in the peristaltic heart, systole
traveled rear-to-front within 60% of the heartbeat period. In the synchronous
heart, systole traveled front-to-rear to segment 17 within about 30% of the
heartbeat cycle. Note that of the 32 heart segments, only a fraction are in
systole at any given time; the others, in diastole, may serve as a conduit
(see text).
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Fig. 7. Long-term optical recordings were used to assess volume differences in the
hearts with respect to coordination mode. Recordings are from heart segments
4, 6, 8 and 10 (A) and from heart segments 13–16 (B) on both sides
(peristaltic mode, shaded boxes; synchronous mode, no shading). Small arrows
denote emptying (A, left heart, segment 10; B, left heart segment 13). In the
top panel, dotted lines ease visualization of the characteristic
intersegmental phase differences in the two modes. We assessed the
end-diastolic volume as the maximum amplitude of the optical signal and the
pumped volume during one cardiac cycle as the area under the curve (shaded
areas in A, left heart). Heart segments 4–10 carry less blood in the
synchronous mode than in the peristaltic mode. (B) Two switches in
coordination mode are shown for posterior heart segments to emphasize the
regular timing of constrictions as well as the precipitous and reciprocal
switches in these quiescent leeches (different animal from that in A). Note
that the posterior heart segments constrict nearly simultaneously (see text
and Fig. 6). The differences in
pumped and end-diastolic blood volume were less obvious in segments
14–16. (C) Ratio of the total blood volume pumped (squares) and the
end-diastolic volume (diamonds) in the synchronous vs the peristaltic
coordination mode from four animals. A ratio of 1 (horizontal dotted line)
indicates no volume difference between coordination modes. Values are means
± s.d., with the number of preparations for each segment given in
parentheses.
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Fig. 8. (A) The latero-dorsal arches shunt blood from the dorsal vessel to the
hearts, with a bias towards the peristaltic heart. Optical recordings are from
segment 14 from the left (black line) and right (brown line) heart and from
the latero-dorsal arches in the left and right hemisegment. (B) Analysis
windows drawn around the vessels and the color code of the optical signals.
Initially, the left heart is in the synchronous mode. Systole of the
latero-dorsal arches in the left hemisegment (double-headed arrow), coincides
with filling of both hearts (rapid downward deflection). After the switch, the
now peristaltic left heart fills when the arches on the contralateral
(synchronous) side enter systole (double-headed arrow). Conversely, systole of
the latero-dorsal arches in the right hemisegment (double-headed arrows) after
its switch into the synchronous mode coincides with filling of the
contralateral, now peristaltic, heart. Additional filling occurs in the
peristaltic heart when the latero-dorsal arch in its own hemisegment enters
systole (arrows) but note that systole in the arches on the peristaltic side
occurs during systole of the synchronous heart and thus is unable to
contribute to its filling.
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© The Company of Biologists Ltd 2007
