A New Look at Insect Respiration

Abstract

A novel thermographic method has been used for simultaneously monitoring the passage of air through up to eight spiracles of endopterygote insects. Measurements on pupae of various lepidopteran species revealed active regulation of inspirations and expirations through one or two spiracles while the majority remained hermetically closed for prolonged periods. Because of subatmospheric hemocoelic pressure acting bellows-like on the large tracheae and air sacs, air is quickly sucked into the tracheal system whenever a spiracle opens. Large, mechanically produced positive peaks in hemocoelic pressure are associated with periodic outbursts of tracheal gases through specific spiracles. During the rhythmic pulsations in hemocoelic pressure, some spiracles open and close at different locations so that CO2 is quickly ventilated. Spiracles on the same segment can function in synchrony with a spiracle on some other, even distant segment. In the period of subatmospheric hemocoelic pressure, the spiracles usually open in "twinkles" or flutters lasting only 50-300 ms. Some pupae, for example, diapausing Manduca, use only one "master spiracle" which opens for 200 ms about once a minute. Each opening is accompanied by a gulp of 500 nl of air sucked in by negative tracheal pressure. All other spiracles may be hermetically closed for 16 h or more.It is concluded that insect respiration is controlled by a hitherto unknown, brain independent, neuromuscular mechanism (coelopulse) consisting of two main components: (a) a mechanism that integrates proprioceptive input to control the location and timing of the spiracular openings, and (b) a coordinated system of hemocoelic pressure control that regulates the force and direction of air flow through the spiracles. The results of this study question the general validity of the classical theory of insect respiration by simple gaseous diffusion.