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Insects breathe discontinuously to avoid oxygen toxicity

Abstract

The respiratory organs of terrestrial insects consist of tracheal tubes with external spiracular valves that control gas exchange. Despite their relatively high metabolic rate, many insects have highly discontinuous patterns of gas exchange, including long periods when the spiracles are fully closed. Two explanations have previously been put forward to explain this behaviour: first, that this pattern serves to reduce respiratory water loss1, and second, that the pattern may have initially evolved in underground insects as a way of dealing with hypoxic or hypercapnic conditions2. Here we propose a third possible explanation based on the idea that oxygen is necessary for oxidative metabolism but also acts as a toxic chemical that can cause oxidative damage of tissues even at relatively low concentrations. At physiologically normal partial pressures of CO2, the rate of CO2 diffusion out of the insect respiratory system is slower than the rate of O2 entry; this leads to a build-up of intratracheal CO2. The spiracles must therefore be opened at intervals to rid the insect of accumulated CO2, a process that exposes the tissues to dangerously high levels of O2. We suggest that the cyclical pattern of open and closed spiracles observed in resting insects is a necessary consequence of the need to rid the respiratory system of accumulated CO2, followed by the need to reduce oxygen toxicity.

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Figure 1: The rate of release of CO2 from a pupa of Attacus atlas over time.
Figure 2: The discontinuous gas exchange cycle (DGC) in a pupa of A. atlas.
Figure 3: Respiratory regulation in pupae of A. atlas during the flutter phase at different atmospheric O2 concentrations.
Figure 4: Intratracheal p O 2 in pupae of A. atlas during the flutter phase as a function of external O2 concentration.

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Acknowledgements

We thank N. Heisler for comments and for providing equipment. T.J.B. would like to thank N. Heisler for his hospitality during a research visit. This work was supported by an NSF grant to T.J.B.

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Correspondence to Timothy J. Bradley.

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Hetz, S., Bradley, T. Insects breathe discontinuously to avoid oxygen toxicity. Nature 433, 516–519 (2005). https://doi.org/10.1038/nature03106

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