A test of the oxidative damage hypothesis for discontinuous gas exchange in the locust Locusta migratoria

Abstract

The discontinuous gas exchange cycle (DGC) is a breathing pattern displayed by many insects, characterized by periodic breath-holding and intermittently low tracheal O 2 levels. It has been hypothesized that the adaptive value of DGCs is to reduce oxidative damage, with low tracheal O 2 partial pressures (PO 2 ∼2-5 kPa) occurring to reduce the production of oxygen free radicals. If this is so, insects displaying DGCs should continue to actively defend a low tracheal PO 2 even when breathing higher than atmospheric levels of oxygen (hyperoxia). This behaviour has been observed in moth pupae exposed to ambient PO 2 up to 50 kPa. To test this observation in adult insects, we implanted fibre-optic oxygen optodes within the tracheal systems of adult migratory locusts Locusta migratoria exposed to normoxia, hypoxia and hyperoxia. In normoxic and hypoxic atmospheres, the minimum tracheal PO 2 that occurred during DGCs varied between 3.4 and 1.2 kPa. In hyperoxia up to 40.5 kPa, the minimum tracheal PO 2 achieved during a DGC exceeded 30 kPa, increasing with ambient levels. These results are consistent with a respiratory control mechanism that functions to satisfy O 2 requirements by maintaining PO 2 above a critical level, not defend against high levels of O 2 .

Gas exchange patterns and water loss rates in the Table Mountain cockroach,Aptera fusca(Blattodea: Blaberidae)

“…This may indicate an overall insensitivity of the species to oxygen variation, which may be of further interest itself in light of the oxidative damage hypothesis of DGE (e.g. Hetz and Bradley, 2005;Boardman et al, 2012;Matthews et al, 2012).…”

Hypotheses regarding the discontinuous gas exchange cycle (DGC) of insects

“…Furthermore. Matthews et al [30 ] used fiber-optic oxygen optodes to observe tracheal PO 2 in locusts and found that locusts maintained a low tracheal PO 2 near 3.4-1.4 kPa in normoxic or hypoxic (10% O 2 ) conditions. However, when placed in hyperoxic environments, these insects did not maintain a PO 2 any lower than 30 kPa, therefore challenging the idea that tracheal hypoxia is beneficial in hyperoxic environments.…”

Discontinuous gas exchange exhibition is a heritable trait in speckled cockroaches Nauphoeta cinerea

“…Recent experimental and comparative studies have lent their support to the hygric and oxidative‐damage hypotheses (Hetz & Bradley, ; Marais et al ., ; White et al ., ; Terblanche et al ., ; Schimpf et al ., , ; Williams et al ., ; Matthews & White, ). Others, on the other hand, have yielded results to the contrary (Contreras & Bradley, ; Boardman et al ., ; Matthews et al ., ), and no hypothesis enjoys unopposed support.…”