Discontinuous respiration in insects—IV. Changes in intratracheal pressure during the respiratory cycle of silkworm pupae☆

Pupae of Hyalophora cecropia have no active respiratory movements except those of the spiracular valves, yet they have discontinuous respiration. Carbon dioxide is retained and released in bursts during brief periods of spiracular opening. Between bursts, O2 enters much faster than CO2 leaves. To determine how the spiracles retain CO2 but permit O2 entry, a number of techniques were devised to measure the barometric pressure of the tracheal system during the respiratory cycle. Several thousand pressure measurements revealed cyclical changes corresponding to the burst cycle. In a typical pupa with a 1 hr cycle, the intratracheal pressure at a burst was within 0·005 mm Hg of atmospheric pressure, tracheal pCO2 was 18·2 per cent and tracheal pCO2 was 3·1 per cent. When the spiralces closed, pressure fell during 10 min to 3·5 mm Hg below atmospheric, tracheal pO2 fell to 2·9 per cent and tracheal pCO2 increased slightly. In response to low tracheal pO2 the spiracles began to flutter and the intratracheal barometric pressure rose stepwise to within 0·3 mm Hg of atmospheric. Intratracheal pressure fluctuated about atmospheric throughout the flutter period until the next burst. An examination of the flutter period revealed that it consisted of hundreds of abbreviated cycles of falling and rising intratracheal pressure. Each of these ‘microcycles’ lasted for 0·3−2 min and the negative pressures developed in them varied from about −0·05 to 0·3 mm Hg. Each microcycle terminated in a miniature burst during which the intratracheal barometric pressure returned to atmospheric. During the flutter period tracheal pO2 remained at about 3·1 per cent. Tracheal pCO2, however, slowly increased to 6·4 per cent and finally triggered the spiracles to open in another burst. Intratracheal barometric pressure then rose to atmospheric, tracheal pO2 rose to 18 per cent and tracheal pCO2 fell to 3 per cent. The burst cycle then began anew. In an atmosphere of 60 per cent O2, the cycle was exaggerated and tracheal barometric pressure dropped as low as 10 mm Hg below atmospheric. These results provide the first direct and repeated measurements of the barometric pressure within an insect's tracheal system. They demonstrate that two sorts of intratracheal vacuums develop in silkworm pupae: large sustained vacuums during the period of prolonged spiracular constriction following each burst and small transient vacuums during the flutter period. As a consequence of these vacuums convective transfer of gases occurs and gases enter the pupae not only by diffusion but by mass transfer. The kinetics of gas exchange was measured during the respiratory cycle by measuring the net gas exchange. These data corroborated conclusions drawn from intratracheal pressure data and from analyses of tracheal gases. The data are considered in relation to Buck's theory of discontinuous respiration and to observations of other workers. The results confirm some essential elements of Buck's theory but the actual mechanisms of discontinuous respiration are shown to be different than the one he proposes. It is shown that there are two distinct mechanisms for producing discontinuous respiration—one characterized by valve constriction and the other by spiracular valve fluttering. The significance of tracheal vacuums in other insects is also discussed, and it is concluded that the gas exchange of many insects without active ventilation movements may be supplemented to a significant degree by suction. The results are also examined in relation to studies of mass transfer of gases in plants.