Discontinuous gas exchange: New perspectives on evolutionary origins and ecological implications

Abstract

1.When at rest, many insects and some other arthropods exchange gasses discontinuously. Whether or not discontinuous gas exchange (DGE) is adaptive has long been controversial. Several competing evolutionary hypotheses exist, none of which enjoy unequivocal support. This Gordian knot seems now to have been cut. 2.Discontinuous gas exchange appears to arise as a consequence of energy-saving, metabolic downregulation. Moreover, many ecological circumstances, such as quiescence during daily inactivity and during seasonal resource shortages, are likely to have favoured such downregulation. 3.Once the brain relinquishes control of gas exchange to the segmental ganglia, an interaction between peripheral CO2 sensing and central O2 sensing sets in, leading to the discontinuous pattern. 4.The evolution of DGE may thus be readily explained, with the primary evolutionary hypothesis incorporating a non-adaptive mechanistic component and an adaptive energy savings one. 5.Paradoxically, though, DGE results in a comparatively high water loss for a given metabolic rate in insects compared with other organisms. Thus, the pattern itself may not have evolved to limit water loss under xeric conditions. Rather, variation in the components of the DGE cycle, which has formed the foundation for much debate concerning the ecological and evolutionary advantages of this gas exchange pattern, may have evolved to do so, accounting for associations between these components and environmental conditions. 6.The relatively high respiratory water loss of insects may spell ecological trouble given increasing metabolic rates of ectotherms associated with rising global temperatures and global change-type drought in many regions. © 2011 The Author. Functional Ecology © 2011 British Ecological Society.