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. 2019 Apr 15;9(1):6075.
doi: 10.1038/s41598-019-42504-3.

Functional Compartmentalization in the Hemocoel of Insects

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Free PMC article

Functional Compartmentalization in the Hemocoel of Insects

Hodjat Pendar et al. Sci Rep. .
Free PMC article

Abstract

The insect circulatory system contains an open hemocoel, in which the mechanism of hemolymph flow control is ambiguous. As a continuous fluidic structure, this cavity should exhibit pressure changes that propagate quickly. Narrow-waisted insects create sustained pressure differences across segments, but their constricted waist provides an evident mechanism for compartmentalization. Insects with no obvious constrictions between segments may be capable of functionally compartmentalizing the body, which could explain complex hemolymph flows. Here, we test the hypothesis of functional compartmentalization by measuring pressures in a beetle and recording abdominal movements. We found that the pressure is indeed uniform within the abdomen and thorax, congruent with the predicted behavior of an open system. However, during some abdominal movements, pressures were on average 62% higher in the abdomen than in the thorax, suggesting that functional compartmentalization creates a gradient within the hemocoel. Synchrotron tomography and dissection show that the arthrodial membrane and thoracic muscles may contribute to this dynamic pressurization. Analysis of volume change suggests that the gut may play an important role in regulating pressure by translating between body segments. Overall, this study suggests that functional compartmentalization may provide an explanation for how fluid flows are managed in an open circulatory system.

Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Representative hemolymph pressure traces in the abdomen and thorax of the beetle Zophobas morio. The hemolymph pressure differs substantially only between the abdomen and thorax, and not within the same segment. (A) TT (thorax-thorax): left and right sides of thorax. The small peaks likely represent the heartbeat. (B) AA (abdomen-abdomen): left and right side of the abdomen. (C) AT (abdomen-thorax): abdomen and thorax. Note also the small pulses in the abdomen without a corresponding pulse in the thorax.
Figure 2
Figure 2
Sample recorded pressures from the left (L) and right (R) sides of abdomen. (A) The recorded pressure from different points of the abdomen show rhythmic patterns of pressure in different points of the abdomen. However, when the animal moves, a non-rhythmic pattern is generated, which was excluded from analysis. (B) The tX-line is a horizontal line that is X% of the pressure amplitude above the base line. Because the baseline of the signals were noisy, we could not accurately determine the start and end of the pressure pulses, and instead used the t50 line to quantify the duration of each pulse.
Figure 3
Figure 3
Comparison of the magnitude of the pressure pulses in the two simultaneously recorded locations. TT: thorax-thorax, AA: abdomen-abdomen, AT: abdomen-thorax; numbers indicate the individual beetle specimens. A line was fitted to the data points at each trial using the Deming method and compared with the P1 = P2 line, which indicates a uniform pressure distribution.
Figure 4
Figure 4
Abdominal movements versus pressure change in the abdomen and thorax. (A) 115 equally spaced points (q1 to q115), representing 25 on the metathorax and 90 on the abdomen, were tracked frame by frame. (B,C) Each pressure pulse in the abdomen and thorax was coincident with a movement of the abdomen. When all the tergites compressed simultaneously (C1), the pressure in both the abdomen and thorax increased. When the first two tergites compressed ventrally (C2), only the pressure in the abdomen increased, without a significant change in the pressure of the thorax. No significant pressure change was observed when a peristaltic wave propagated posteriorly (C3).
Figure 5
Figure 5
Distribution of the tracheae across the body of the beetle Zophobas morio. This volumetric analysis was based on 3700 tomographic images from one individual, representing tracheae of diameter greater than 5 µm; smaller tracheae and tracheoles could not be resolved in the x-ray images and were not included. The volume of tracheae is greatest in the meso- and metathorax, where the flight muscles are concentrated. About 35% of the tracheal volume is in the abdomen.
Figure 6
Figure 6
Morphology that may contribute to internal compartmentalization. The cuticle between the abdomen and thorax may function to isolate the thorax from the abdomen. (A) This cuticle is located posteriorly to the hind coxae, between the abdomen and thorax. (B) To observe this cuticle the wings were removed and (C) the beetle was bent dorsally. (D) Cutting the abdomen helps to see the cuticle more clearly. It also reveals a channel between the abdomen and thorax, which is filled with the esophagus. (E) This cuticle and the gap between the abdomen and thorax can be observed in tomographic images as well.
Figure 7
Figure 7
Large muscles in the thorax increase the impedance for hemolymph movement. The large gut of the beetles passes through the thoracic muscles. Any local increase in the volume of the gut would increase the impedance and possibly block the hemolymph passages. The area of the hemolymph around the gut is less than 35% of the gut area in some points of the thorax.

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