Correlated patterns of tracheal compression and convective gas exchange in a carabid beetle

Abstract

Rhythmic tracheal compression is a prominent feature of internal dynamics in multiple orders of insects. During compression parts of the tracheal system collapse, effecting a large change in volume, but the ultimate physiological significance of this phenomenon in gas exchange has not been determined. Possible functions of this mechanism include to convectively transport air within or out of the body, to increase the local pressure within the tracheae, or some combination thereof. To determine whether tracheal compressions are associated with excurrent gas exchange in the ground beetle Pterostichus stygicus, we used flow-through respirometry and synchrotron x-ray phase-contrast imaging to simultaneously record CO(2) emission and observe morphological changes in the major tracheae. Each observed tracheal compression (which occurred at a mean frequency and duration of 15.6+/-4.2 min(-1) and 2.5+/-0.8 s, respectively) was associated with a local peak in CO(2) emission, with the start of each compression occurring simultaneously with the start of the rise in CO(2) emission. No such pulses were observed during inter-compression periods. Most pulses occurred on top of an existing level of CO(2) release, indicating that at least one spiracle was open when compression began. This evidence demonstrates that tracheal compressions convectively pushed air out of the body with each stroke. The volume of CO(2) emitted per pulse was 14+/-4 nl, representing approximately 20% of the average CO(2) emission volume during x-ray irradiation, and 13% prior to it. CO(2) pulses with similar volume, duration and frequency were observed both prior to and after x-ray beam exposure, indicating that rhythmic tracheal compression was not a response to x-ray irradiation per se. This study suggests that intra-tracheal and trans-spiracular convection of air driven by active tracheal compression may be a major component of ventilation for many insects.