Insect gas exchange patterns: a phylogenetic perspective

Abstract

SUMMARY Most investigations of insect gas exchange patterns and the hypotheses proposed to account for their evolution have been based either on small-scale,manipulative experiments, or comparisons of a few closely related species. Despite their potential utility, no explicit, phylogeny-based, broad-scale comparative studies of the evolution of gas exchange in insects have been undertaken. This may be due partly to the preponderance of information for the endopterygotes, and its scarcity for the apterygotes and exopterygotes. Here we undertake such a broad-scale study. Information on gas exchange patterns for the large majority of insects examined to date (eight orders, 99 species)is compiled, and new information on 19 exemplar species from a further ten orders, not previously represented in the literature (Archaeognatha,Zygentoma, Ephemeroptera, Odonata, Mantodea, Mantophasmatodea, Phasmatodea,Dermaptera, Neuroptera, Trichoptera), is provided. These data are then used in a formal, phylogeny-based parsimony analysis of the evolution of gas exchange patterns at the order level. Cyclic gas exchange is likely to be the ancestral gas exchange pattern at rest (recognizing that active individuals typically show continuous gas exchange), and discontinuous gas exchange probably originated independently a minimum of five times in the Insecta.

Scaling of gas exchange cycle frequency in insects

“…The significant difference in intercepts is probably due to the lower metabolic rate in DGE versus CGE. A much weaker difference in slope, which was not included in the best-fit model, might represent the outcome of selection for DGE, the derived condition in insects (Marais et al 2005). Lower f C at smaller sizes might affect respiratory water savings in the same way as longer DGE cycles do in animals from xeric environments (Chown & Davis 2003;White et al 2007).…”

Terrestrial Insects with Tracheae Breath by Actively Regulating Ventilatory Movements: Physiological Similarities to Humans

“…From 1960 onwards, the mainstream research on insect respiration has been directed to very sensitive instruments for flow-through, infrared analysis of CO2 (reviewed by Lighton 1996Lighton , 1998Lighton , 2008Marais et al 2005;Bradley 2005, Chown et al 2006). In these experiments, ants or termites, adapted to live in nests or burrows under conditions of balanced humidity and CO2 content, were exposed to an unnatural stream of desiccating scrubbed air (0% CO2, 0% H2O) to measure their CO2 release.…”

“…The DGC model based on the diffusional theory of Krogh is composed of three stereotypically repeated phases: a) open spiracle-CO2 outbursts; b) closed spiracles, and; c) fluttering spiracles (OCF cycles). This mechanical concept of discontinuous respiratory cycles is still used as a theoretical basis of insect respiration (Lighton 1996(Lighton , 1998Marais et al 2005;Hetz and Bradley 2005;Contreras and Bradley 2009;Chown et al 2006;Klowden 2013). The authors of these papers speak about open, closed, or fluttering spiracles without the slightest experimental evidence about real performance of the spiracular valves.…”

“…This statement conflicts with the widely used diffusional theory of insect respiration, which was created almost 100 years ago (Krogh 1920). Due to the lack of experimental data, the theory has persisted as the main model of insect respiration until this time (Krogh 1941;Lighton 1996Lighton , 2008Wasserthal 1996;Nation 2002;Marais et al 2005;Westneat 2003Westneat , 2008Chown et al 2006;Hetz and Bradley 2005;Contreras and Bradley 2009;Aboelkassem and Staples 2013;Klowden 2017). Our results corroborate previous findings of Sláma (1984,1988,1999,2010), which provided experimental evidence that large or small insects actively ventilated the tracheal system by the mechanical inhalation or exhalation of air through selected spiracles.…”

Discontinuous gas-exchange cycle characteristics are differentially affected by hydration state and energy metabolism in gregarious and solitarious desert locusts

“…Indeed, they have only been reported, to date, in seven insect orders: Lepidoptera, Coleoptera, Hymenoptera, Blattodea, Orthoptera, Hemiptera and Diptera, (Marais et al, 2005;Gray and Bradley, 2006;Contreras and Bradley, 2009), in addition to other tracheated arthropods, such as centipedes, ticks and solifuges (Chown, 2011). Moreover, in insects that do exhibit DGCs, the pattern is reported to be limited to periods of quiescence (e.g.…”