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First published online October 19, 2007
Journal of Experimental Biology 210, 3707-3719 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.007864

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Drosophila flies combine periodic heartbeat reversal with a circulation in the anterior body mediated by a newly discovered anterior pair of ostial valves and `venous' channels

Lutz T. Wasserthal

Institute of Biology, University of Erlangen-Nuernberg, Staudtstrasse 5, D-91058 Erlangen, Germany

View larger version (65K): [in this window] [in a new window]   Fig. 1. Setup for recording heartbeat in Drosophila. (A) IR sensor-chip with adjusted holder supporting the fly. (B) D. melanogaster in the measuring position calmed down by holding a plastic ball. Arrow indicates the unused part of the sensor line.

View larger version (15K): [in this window] [in a new window]   Fig. 2. Illustration demonstrating orientation of the IR-light beam and the opposite five sensor elements (1–5) for recording pulsations of the anterior heart (second segment) in D. melanogaster. Proportions to scale.

View larger version (26K): [in this window] [in a new window]   Fig. 3. Survey of heartbeat reversals, recorded by the IR-sensor beside the second abdominal segment. Black bars represent the periods of retrograde heart pulses. (A) Regular repetition of heartbeat reversals and intermittent bouts of abdominal contractions (D. hydei, male 3). (B) Series of three heartbeat periods in D. melanogaster (female 2). During retrograde pulses the mean transmittance level is higher than during forward pulses.

View larger version (62K): [in this window] [in a new window]   Fig. 4. Heartbeat reversals in D. hydei (female 6). The pulse sequences of three traces are sampled at 2000 Hz and the different mean levels of transmission are equalized by use of a high-pass filter of 0.5 Hz. (A) Survey of two series of heartbeat periods. (B,C) Shorter time periods with individual heart pulses. Detail from the boxes marked in A. The metachronous delay of the pulse wave is recorded by three sensor elements along the abdominal segment 3 (green), inter-segmentally (black) and segment 2 (red). (B) Anterograde pulses show typically a double peak (arrowheads) or even further peaks (asterisk). (C) Retrograde pulses show only one peak. The peak of highest transmission corresponds to the moment when the heart is maximally distended by the presystolic wave. To illustrate the metachrony of the pulse wave, the maximum peaks are connected (dotted lines) and the resulting intervals are projected as a bar on the x-axis. Green anterograde, red retrograde.

View larger version (23K): [in this window] [in a new window]   Fig. 5. Directional change of heartbeat, analyzed by the metachrony along five sensor sites in D. melanogaster (female 2). (A) Transition from anterograde to retrograde beating. Arrowheads indicate double peaks during diastole. (B) Transition from retrograde to anterograde beating. The first anterograde pulse collides with a retrograde pulse at the anterior sensor point (asterisk). Explanations as in Fig. 4.

View larger version (12K): [in this window] [in a new window]   Fig. 6. Comparison of periodic heartbeat traces of first with third heart segment in D. hydei (male 4). (A) Sensor beside the waist at the transition of the first heart segment to the aorta. The mean IR-transmittance is decreasing during retrograde pulsations, when no hemolymph is pumped through the aorta. Pulses, probably of the intestine, with a lower frequency are superimposed on the heart pulses (arrows). (B) Same individual, with sensor beside the third heart segment the next day. Mean IR-transmittance is increasing during retrograde pulsations, when hemolymph is accumulating in the abdomen.

View larger version (8K): [in this window] [in a new window]   Fig. 7. Influence of restrained abdomen tip on the heart pulses in D. hydei (female 3). This form of pulsewise alternating heartbeat reversals can last for hours as long as the abdomen is prevented from length changes. It documents the importance of the role of abdomen for regular heartbeat periodicity.

View larger version (105K): [in this window] [in a new window]   Fig. 8. Anatomy of the heart and its incurrent and excurrent openings in D. melanogaster. (A) Light micrograph of the entire heart, ventral view. Ostia 2, 3 and 4 (O2, O3, O4) are clearly visible through the transparent dorsal diaphragm. Fat body (FB) and pericardial cells (PC) cover the posterior part of the heart. DLM, dorso-longitudinal flight muscles attached to the mesophragma (Ph II). (B–E) SEMs. (B) Ventral view of the entire heart. The dorsal diaphragm (DD) with its longitudinal muscles is visible, covering the ventral surface of the heart. The excurrent opening (EO) is visible between the pair of caudal suspending muscles. AM, alary muscles. (C) Longitudinal cut of anterior heart chamber with first ostium (O1). Anterior (Ant OC) and posterior valve cells (Post OC) protrude into the heart lumen. (D) Third ostium with closed valve lips. (E) Caudal end of the heart with excurrent opening, suspending muscles severed to expose the relaxed opening and the connective tissue strands (CT).

View larger version (176K): [in this window] [in a new window]   Fig. 9. Horizontal semithin sections of the first abdominal segment/posterior thorax in D. hydei. (A) Section just below the first abdominal tergite, showing the heart chamber (H1) with first ostia (O1) and venous channel (VC) bordered by a cuticular septum (CS), pericardial diaphragm (PD) and constitutive fat tissue (CFB). (B) Section 32 µm below A, showing the venous channel and the tergo-pleural muscle (M) attached to the cuticular septum. (C) Section 30 µm below B. The aorta (Ao) is collapsed. The venous hemolymph channel is bordered by the tergo-pleural muscle. (D) Tubular tergo-pleural muscle. Detail similar to C. (E) Section 180 µm below B at the basis of the haltere (Ha). (F) Section 268 µm below B. Venous channel above the metathoracic spiracle (Sp II). The tergo-pleural muscle (M) is close near the pleural septum (PS), where it is attached 98 µm more ventrally. FB, fat body; I, intestine; Ph II, mesophragma; T, trachea.

View larger version (101K): [in this window] [in a new window]   Fig. 10. The venous space (VS) and its connection to the anterior heart (H) in the first abdominal segment in D. melanogaster. View towards the mesophragma (Ph II). (A,B,D,E) SEMs; (C) light microscopy. (A) Opened anterior heart chamber, surrounded by the pericardial diaphragm (PD) and the fat body (FB). (B) Detail from A, showing the protruding valve cells of the first ostium. (C) Light micrograph of the first abdominal segment, showing the tergo-pleural muscles (M), pericardial diaphragm (PD) and aorta (Ao). Sectioned at the level of the posterior end of the (collapsed) conical heart chamber (H). Most fat body (FB) on the left side is removed. (D) NaOH-maceration preparation of the anterior abdomen. Cuticular ridge (CR), arising from the posterior metanotum and giving rise to the cuticular septum (CS), bordering the venous channel. (E) View as in D after removal of the pericardial diaphragm to show the anterior heart attachment by connective tissue strands (CT) and opening of the venous channel. PD, tissue remnants of the pericardial diaphragm. (F) Schematic illustration of components involved in hemolymph transport of the anterior heart.). Ant OC, anterior ostial valve cell; AS 1, first abdominal segment; FG, fat granule; M, tergo-pleural muscle; O1, first ostium; Post OC, posterior valve cell; PS, pleural septum; VC, venous channel; VF, ventral foramen; VS, venous space.

View larger version (14K): [in this window] [in a new window]   Fig. 11. Schematic drawing of the heart with its ostia and the dorsal diaphragm in Drosophila. (A) Dorsal view, (B) lateral view. O1–O5, incurrent ostia of abdominal segments 1–5; Ph II, mesophragma.

View larger version (23K): [in this window] [in a new window]   Fig. 12. Graph summarizing hemolymph circulation through the forward (A,B) and backward beating heart (C,D). (A,C) Overview; (B,D) detail, showing the central location of the anterior heart and its strategically favourable connection to the venous channels (VC). The lateral thoracic hemolymph flows through these channels directly to the first ostia. During diastole of the backward beating heart, thoracic hemolymph enters these anterior ostia exclusively. During forward beating, hemolymph is aspired from the heart through all ostia, including the first ones. Thus a lateral circulation in the thorax is maintained independently of heartbeat direction. S, pericardial septum.