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

Abstract

The operation of the thoracic spiracular valves was analysed using anatomical and physiological techniques. Dense spiracular filter trichomes impede a diffusive gas exchange. However, the hinged posterior filter flap of the metathoracic spiracle (Sp2) opens passively during upstroke of the wings and closes by the suction of the subatmospheric tracheal pressure during the downstroke, which supports a unidirectional respiratory airflow. The action of the interior spiracular valve lids was recorded by photocell sensors oriented above the enlarged spiracles and projected onto the screen of a video camera. The thoracic spiracles opened much quicker (approximately 0.1 s) than they closed (1 s), suggesting that the spiracular muscles are openers, as confirmed by experimental induction of muscle contraction. Simultaneous photocell measurement revealed that the first and second thoracic spiracles act concordantly. At rest, the spiracles were mostly closed or only slightly open (<1%). During intermittent short flights, the valves opened wide at the start of the flight for a short time, and in many cases opened again after the flight ended. Often, the opening was wider after the flight ended than during the flight itself. During long spontaneous continuous flight phases (up to 2 h), the valves were only slightly open (<5%), widening shortly after transient increases of wing stroke intensity. It is an amazing paradox that the spiracles were only slightly open when the requirement for O 2 was high during sustained flight. The advantage of generating sub-atmospheric pressure, supporting a unidirectional airflow with a P O2 increase above the resting level, is discussed.

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

“…Our explanation for a preference of ventilatory over diffusive principle in insect respiration is underlined by two main factors: a) restraining respiratory acidaemia by enzymatic hydration of carbonic acid, which is associated with a bulk outflow of the produced, highly concentrated CO2 through the nearest spiracle, and; b) resorption and retention of water within the antiadhesive internal coating of the tracheal system. It was known for a long time (Babák 1921, Kuznetzoff 1953, that insect spiracles were protected against gas diffusion by sophisticated spiracular slits, sieves, foam and narrow atria, which has been recently confirmed by Wasserthal and Fröhlich (2017) who described antidiffusive spiracular trabeculae and spines.…”

“…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.…”

Comparative Anatomy of the Insect Tracheal System Part 1: Introduction, Apterygotes, Paleoptera, Polyneoptera

“…Wigglesworth's landmark The Principles of Insect Physiology discusses insect respiration in some detail, including tracheal development, differences in spiracular control, fluid filling of tra-cheoles, water loss, and even respiration in endoparasitic insects (Wigglesworth, 1972). Numerous studies have investigated directional airflow, primarily related to insect flight and even including valve mechanisms (Vinal, 1919;Weis-Fogh and Jensen, 1956;Weis-Fogh, 1967;Harrison et al, 2013;Wasserthal, 2015;Wasserthal and Frohlich, 2017;Wasserthal et al, 2018). Additionally, the assumption that insects do not require respiratory proteins was recently shown to be invalid, with the discovery of the expression of hemoglobins in all insect orders (Herhold et al, 2020).…”

Adult and Larval Tracheal Systems Exhibit Different Molecular Architectures in Drosophila

“…The more complex adult tracheal system comprises compressible air sacs and many anastomoses to allow for active breathing movement [ 4 ]. Recent studies have given us a basic understanding of how these very complex organs allow a highly efficient gas exchange that matches the metabolic needs during maximal physical activity [ 5 , 6 , 7 , 8 , 9 ]. While functional studies were mostly conducted with large insects, such studies are rare in the model insect, the fruit fly Drosophila melanogaster .…”