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

Abstract

The termination of discontinuous gas exchange cycles (DGCs) in severely dehydrated insects casts doubt on the generality of the hygric hypothesis, which posits that DGCs evolved as a water conservation mechanism. We followed DGC characteristics in the two density-dependent phases of the desert locust Schistocerca gregaria throughout exposure to an experimental treatment of combined dehydration and starvation stress, and subsequent rehydration. We hypothesized that, under stressful conditions, the more stressresistant gregarious locusts would maintain DGCs longer than solitary locusts. However, we found no phase-specific variations in body water content, water loss rates (total and respiratory) or timing of stress-induced abolishment of DGCs. Likewise, locusts of both phases re-employed DGCs after ingesting comparable volumes of water when rehydrated. Despite comparable water management performances, the effect of exposure to stressful experimental conditions on DGC characteristics varied significantly between gregarious and solitary locusts. Interburst duration, which is affected by the ability to buffer CO 2 , was significantly reduced in dehydrated solitary locusts compared with gregarious locusts. Moreover, despite similar rehydration levels, only gregarious locusts recovered their initial CO 2 accumulation capacity, indicating that cycle characteristics are affected by factors other than haemolymph volume. Haemolymph protein measurements and calculated respiratory exchange ratios suggest that catabolism of haemolymph proteins may contribute to a reduced haemolymph buffering capacity, and thus a compromised ability for CO 2 accumulation, in solitary locusts. Nevertheless, DGC was lost at similar hydration states in the two phases, suggesting that DGCs are terminated as a result of inadequate oxygen supply to the tissues.

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.…”

An experimental evolution study confirms that discontinuous gas exchange does not contribute to body water conservation in locusts

“…A breakdown of the cycle into its burst and interburst phases (figure 1a) revealed that differences in cycle duration resulted from changes in the interburst (t 68 ¼ 3.790, p , 0.001) but not the burst duration (t 68 ¼ 1.119, p ¼ 0.267). Calculation of CO 2 accumulation during the interburst (see [12]), assuming constant cellular metabolic rate despite intermittent gas exchange with the environment, revealed that the selected locusts had evolved a significantly higher capacity to accumulate CO 2 (F 1,68 ¼ 9.763, p ¼ 0.003) (table 2).…”

“…Furthermore, we found a significantly higher haemolymph protein concentration in the selected locusts (S.T., 2016, unpublished data), and this important haemolymph buffer in locusts [15] may aid in alleviating acid-base balance alterations resulting from CO 2 accumulation. Interestingly, locust density-dependent phase-specific variations in haemolymph protein content were also associated with changes in DGE properties in the desert locust, Schistocerca gregaria, during desiccation [12].…”

Microbiome-related aspects of locust density-dependent phase transition

“…When crowded, however, locusts express the notorious gregarious phenotype, tending to aggregate into swarms, to migrate, and to consume huge amounts of vegetation, thus causing severe damage to agriculture (gregarious phase) [1,3,5,6]. The phase transition from solitary to gregarious in the different locust species encompasses many changes, including a marked behavioral change [5][6][7][8], as well as immense physiological changes [5,6,9,10].…”