Periodic heartbeat reversals cause cardiogenic inspiration and expiration with coupled spiracle leakage in resting blowflies Calliphora vicina R.-D.

Abstract

Summary Respiration in insects is thought to be independent of the circulatory system because insects typically lack respiratory pigments and because oxygen transport occurs in the gaseous phase via a ramified tracheal system by diffusion and convection directly to the tissues. In the blowfly, as in other insects with periodic heartbeat reversal, the haemolymph is periodically shifted between the anterior body and abdomen, exerting alternating pressure changes on the compliant tracheae in the thorax and reciprocally in the abdomen. Simultaneous pressure and O2-optode measurements show that, during negative pressure periods, the tracheal PO2 increases by 0.5 kPa. In the quiescent fly, tracheal PO2 is rather high (17.5–18.9 kPa), although the thoracic spiracles remain constricted. Microscopic video records and reflectance measurements revealed that the dorsal soft edges of the valve lips of the second spiracle leave a very small leak, which is passively widened during backward pulses of the heart. Thus, negative pressure, combined with increased leakage of the Sp2 valve enable inspiration in the thorax. The positive pressure periods are correlated with a new type of convective CO2 micro-bursts as shown in flow-through measurements. The bulk of the CO2 is, however, released after longer interbursts in macro-bursts with valves opening actively reminding of the open phase in a cyclic gas exchange (CGE). When the valves open, the PO2 in the thoracic air sacs unexpectedly drops by a mean of 2.75±1.09 kPa, suggesting a displacement of O2 by the transient accumulation of CO2 in the tracheal system before its release.