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The mechanisms underlying the production of discontinuous gas exchange cycles in insects

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Abstract

This review examines the control of gas exchange in insects, specifically examining what mechanisms could explain the emergence of discontinuous gas exchange cycles (DGCs). DGCs are gas exchange patterns consisting of alternating breath-hold periods and bouts of gas exchange. While all insects are capable of displaying a continuous pattern of gas exchange, this episodic pattern is known to occur within only some groups of insects and then only sporadically or during certain phases of their life cycle. Investigations into DGCs have tended to emphasise the role of chemosensory thresholds in triggering spiracle opening as critical for producing these gas exchange patterns. However, a chemosensory basis for episodic breathing also requires an as-of-yet unidentified hysteresis between internal respiratory stimuli, chemoreceptors, and the spiracles. What has been less appreciated is the role that the insect’s central nervous system (CNS) might play in generating episodic patterns of ventilation. The active ventilation displayed by many insects during DGCs suggests that this pattern could be the product of directed control by the CNS rather than arising passively as a result of self-sustaining oscillations in internal oxygen and carbon dioxide levels. This paper attempts to summarise what is currently known about insect gas exchange regulation, examining the location and control of ventilatory pattern generators in the CNS, the influence of chemoreceptor feedback in the form of O2 and CO2/pH fluctuations in the haemolymph, and the role of state-dependent changes in CNS activity on ventilatory control. This information is placed in the context of what is currently known regarding the production of discontinuous gas exchange patterns.

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Fig. 1

Modified from Matthews and Terblanche (2015)

Fig. 2

Figures modified from (Miller 1981a; Miall and Denny 1886)

Fig. 3
Fig. 4
Fig. 5

Figure from Matthews and White (2011b)

Fig. 6

Locust and cockroach CNS organisation adapted from Niven et al. (2008). Ant CNS from Choi et al. (2009). (1) Bustami and Hustert (2000), (2) Matthews and White (2011b), (3) Myers and Retzlaff (1963), (4) Lighton and Garrigan (1995), (5) Lighton et al. (1993), (6) Lighton (1992), (7) Quinlan and Lighton (1999)

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Acknowledgements

My sincere thanks to Ian Hume for the invitation to write this review, and to the three anonymous reviewers for their comments and constructive criticism that greatly improved an earlier version of this manuscript.

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  1. Department of Zoology, The University of British Columbia, Vancouver, B.C., Canada

    Philip G. D. Matthews

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  1. Philip G. D. Matthews
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Correspondence to Philip G. D. Matthews.

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Communicated by I.D. Hume.

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Matthews, P.G.D. The mechanisms underlying the production of discontinuous gas exchange cycles in insects. J Comp Physiol B 188, 195–210 (2018). https://doi.org/10.1007/s00360-017-1121-6

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  • DOI: https://doi.org/10.1007/s00360-017-1121-6

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