Intricate but tight coupling of spiracular activity and abdominal ventilation during locust discontinuous gas exchange cycles

Abstract

Discontinuous gas exchange (DGE) is the best studied among insect gas exchange patterns. DGE cycles comprise three phases, which are defined by their spiracular state: close, flutter, and open, although spiracle status has rarely been monitored directly. Rather, it is often assumed based on CO2 emission traces. In this study, we directly recorded electromyogram (EMG) signals from the closer muscle of the second thoracic spiracle and from abdominal ventilation muscles in a fully intact locust during DGE. Muscular activity was monitored simultaneously with CO2 emission, under normoxia and under various experimental oxic conditions. Our findings indicate that locust DGE does not correspond well with the commonly described three-phase cycle. We describe unique DGE-related ventilation motor patterns, coupled to spiracular activity. During the open phase, when CO2 emission rate is the highest, the thoracic spiracles do not remain open; rather, they open and close rapidly. This fast spiracle activity coincides with in-phase abdominal ventilation, while alternating with the abdominal spiracle and thus facilitating a unidirectional air flow along the body. A change in the frequency of rhythmic ventilation during the open phase suggests modulation by intra-tracheal CO2 levels. A second, slow-ventilatory-movement pattern probably serves to facilitate effective gas diffusion during spiracle closure. Two flutter-like patterns are described in association with the different types of ventilatory activity. We offer a modified mechanistic model for DGE in actively ventilating insects, incorporating ventilatory behavior and changes in spiracle state.