Oxygen diffusion limitation triggers ventilatory movements during spiracle closure when insects breathe discontinuously

Abstract

During discontinuous gas exchange cycles in insects, spiracular opening follows a typical prolonged period of spiracle closure. Gas exchange with the environment occurs mostly during the period of full spiracular opening. In this study we tested the hypothesis that recently reported ventilatory movements during the spiracle closure period serve to mix the tracheal system gaseous contents, and support diffusive exchanges with the tissues. Using heliox (21% O 2 , 79% He), we found that by increasing oxygen diffusivity in the gas phase, ventilatory movements of Schistocerca gregaria were significantly delayed compared with normoxic conditions. Exposure to hyperoxic conditions (40% O 2 , 60% N 2 ) resulted in a similar delay in forced ventilation. Together, these results indicate that limits to oxygen diffusion to the tissues during spiracle closure trigger ventilatory movements, which in turn support tissue demands. These findings contribute to our understanding of the mechanistic basis of respiratory gas exchange between insect tissues and the environment.

The effect of discontinuous gas exchange on respiratory water loss in grasshoppers (Orthoptera: Acrididae) varies across an aridity gradient

“…2B,C) with VĊ O2 gradually increasing during the interburst in all individuals (Table 1). This suggestion is in agreement with a dominant role for tracheal oxygen transport capacity in shaping DGC characteristics in grasshoppers (Groenewald et al, 2014; see also Huang et al, 2014). Importantly, CO 2 emission during the interburst would be accompanied by emission of water vapour, further increasing losses resulting from longer burst duration.…”

“…We predicted that: (1) DGC prevalence would be positively correlated with habitat aridity; (2) T. pulchripennis would have a longer interburst phase and/or a shorter burst phase compared with the two mesic species; and (3) DGC and variation in its characteristics would be translated to water savings. Tissue oxygen demand and tracheal conductance limiting its supply are major factors affecting gas exchange pattern characteristics in grasshoppers (Groenewald et al, 2014;Huang et al, 2014). Therefore, we measured grasshopper tracheal volume in an attempt to correlate DGC characteristics with potential variation in available oxygen storage volume during the interburst phase.…”

Diffusive flux in a model of stochastically gated oxygen transport in insect respiration

“…Depending on the physiological conditions, insects can enter a regime of discontinuous gas exchange, in which the spiracle appears to be randomly switching between the open and closed states. [25][26][27][28][29] The functional significance of this regime is still unclear, but several of the proposed mechanisms require quantitative analysis of diffusive fluxes through the tracheal network. 25 A first step in this direction was made by Lawley et al 30 who proposed and analyzed a one-dimensional diffusion model, in which the absorbing boundary condition at the tube exit was used to describe oxygen consumption by the tissue, and randomly switching boundary conditions at the tube entrance were used to describe the spiracle dynamics.…”

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

“…Similar tracheal volumes (Table 2) mean that gregarious and solitary locusts do not vary in the magnitude of their oxygen resources once the spiracles are closed. It has recently been shown that S. gregaria complement diffusive oxygen transport to their tissues with active ventilation during the interburst (Huang et al, 2014). A decrease in haemolymph volume and pressure may impair the compression of air sacs and thus compromise ventilatory gas transport in the tracheal system (Harrison et al, 2013), as was also reflected in reduced maximal VĊ O2 values in dehydrated locusts during the burst (Fig.…”