Periodic heartbeat reversals cause cardiogenic inspiration and expiration with coupled spiracle leakage in resting blowfliesCalliphora vicinaR.-D.

Abstract

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 through 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 in the abdomen. Simultaneous pressure and O 2 optode measurements show that, during negative pressure periods, the tracheal partial pressure of oxygen (P O2 ) increases by 0.5 kPa. In the quiescent fly, tracheal P O2 is rather high (17.5-18.9 kPa), although the thoracic spiracles remain constricted. Microscopic video recordings 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 spiracle Sp2 valve enable inspiration in the thorax. The positive pressure periods are correlated with a new type of convective CO 2 micro-bursts as shown in flow-through measurements. The bulk of the CO 2 is, however, released after longer interbursts in macro-bursts with actively opening valves reminiscent of the open phase in a cyclic gas exchange. When the valves open, the P O2 in the thoracic air sacs unexpectedly drops by a mean of 2.75±1.09 kPa, suggesting a displacement of O 2 by the transient accumulation of CO 2 in the tracheal system before its release.

Terrestrial Insects with Tracheae Breath by Actively Regulating Ventilatory Movements: Physiological Similarities to Humans

“…The leading role of heartbeat in tracheal ventilation was later extended to all holometabolous insects (Wasserthal 1996), while the respiratory impact of 100-fold stronger extracardiac pulsations was neglected. In a more recent paper on insect heartbeat and respiration, Wasserthal (2014) stated that: "...periodic heartbeat reversals cause cardiogenic inspiration and expiration with coupled spiracle leakage in resting blowflies." In the most recent paper, Wasserthal and Fröhlich (2017) describe functions of the spiracular valve, using a high-speed video, without attributing a role for extracardiac pulsations.…”

“…The effect of changes in haemocoelic pressure on tracheal ventilation has been well established (Sláma 1988(Sláma , 1999(Sláma , 2009). On the other hand, the assumed effects of heartbeat on regulation of insect respiration (Wasserthal 1996(Wasserthal , 2014 still require additional experimental proof. The reason for more experimental data is that the impact of insect heartbeat on haemocoelic pressure is as a rule up to 100-to 500-fold smaller in comparison with the extracardiac pulsations (Sláma 2009).…”

“…The described physiological mechanism more recently has been corroborated by new electronic methods (Sláma 2009(Sláma , 2010. However, some authors are reluctant to recognize respiratory functions of extracardiac pulsations (Wasserthal 1996(Wasserthal , 2014, and ascribe respiratory functions to the heart, which is a small, tubular organ suspended in haemocoelic cavity, whose anatomical structure and inefficient myogenic functions (with 100-fold smaller impact on haemaocoelic pressure in comparison with the extracardiac pulsations) can hardly affect functions of the tracheal system (Sláma 2009(Sláma , 2010.…”

Structure of the thoracic spiracular valves and their contribution to the unidirectional gas exchange in flying blowfliesCalliphora vicina

“…The spiracle opening behaviour during activity At full rest, the respiratory gas exchange in C. vicina through the thoracic spiracles is facilitated by pressure changes induced by heartbeat reversals and a correlated leakage of the dorsal Sp2 (Wasserthal, 2014). As heartbeat reversals also continue with higher frequency during flight, this mechanism is also operative during flight (Wasserthal, 2015).…”

“…There are visual observations in diapausing silkmoth pupae, locusts and cockroaches, but only few original recordings of the cyclic opening or closing behaviour of the valves (Schneiderman, 1960;Miller, 1973). In several publications, the opening behaviour was concluded from the measured CO 2 and H 2 O release and O 2 uptake in different resting insects (Kestler, 1985;Lighton, 1988Lighton, , 1996Byrne and Duncan, 2003;Jögar et al, 2011;Wasserthal, 2014) or from other respiratory effects like abdominal movements with concurrent tracheal pressure changes (Schneiderman and Schechter, 1966). Anemometric effects were recorded at moth spiracles with thermistors (Wasserthal, 1981;Sláma, 1988).…”