A hierarchy of factors influence discontinuous gas exchange in the grasshopper Paracinema tricolor (Orthoptera: Acrididae)

Abstract

The evolutionary origin and maintenance of discontinuous gas exchange (DGE) in tracheate arthropods are poorly understood and highly controversial. We investigated prioritization of abiotic factors in the gas exchange control cascade by examining oxygen, water and haemolymph pH regulation in the grasshopper Paracinema tricolor. Using a full-factorial design, grasshoppers were acclimated to hypoxic or hyperoxic (5% O 2 , 40% O 2 ) gas conditions, or dehydrated or hydrated, whereafter their CO 2 release was measured under a range of O 2 and relative humidity (RH) conditions (5%, 21%, 40% O 2 and 5%, 60%, 90% RH). DGE was significantly less common in grasshoppers acclimated to dehydrating conditions compared with the other acclimations (hypoxia, 98%; hyperoxia, 100%; hydrated, 100%; dehydrated, 67%). Acclimation to dehydrating conditions resulted in a significant decrease in haemolymph pH from 7.0±0.3 to 6.6±0.1 (mean ± s.d., P=0.018) and also significantly increased the open (O)-phase duration under 5% O 2 treatment conditions (5% O 2 , 44.1±29.3 min; 40% O 2 , 15.8±8.0 min; 5% RH, 17.8±1.3 min; 60% RH, 24.0±9.7 min; 90% RH, 20.6±8.9 min). The observed acidosis could potentially explain the extension of the O-phase under low RH conditions, when it would perhaps seem more useful to reduce the O-phase to lower respiratory water loss. The results confirm that DGE occurrence and modulation are affected by multiple abiotic factors. A hierarchical framework for abiotic factors influencing DGE is proposed in which the following stressors are prioritized in decreasing order of importance: oxygen supply, CO 2 excretion and pH modulation, oxidative damage protection and water savings.

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

“…Hence, unless the effect of dehydration on threshold P CO2 values for spiracular opening (Bursell, 1957;Miller, 1964) varies in the two phases, gregarious locusts should be expected to maintain DGCs for longer. A possible explanation lies in the hierarchy of factors affecting DGC expression and its characteristics (Groenewald et al, 2014). According to the model suggested by those authors, DGCs will be expressed and their characteristics will be determined by acid-base balance considerations, as long as the pattern allows adequate oxygen supply to the tissues.…”

“…Mesic ants exhibited DGCs, whereas a closely related xeric species did not (Lighton and Berrigan, 1995). In addition, grasshoppers and beetles abandoned DGCs following severe dehydration stress, when stricter management of body water stores would be expected Quinlan and Hadley, 1993;Chown and Holter, 2000;Groenewald et al, 2014). Abolishment of DGCs when body water (and haemolymph in particular) is lost can be explained by a reduced CO 2 buffering capacity during spiracle closure, before the spiracles open again and allow CO 2 washout (Lighton, 1996).…”

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

“…However, habitat aridity could provide extra selective pressure, whichwould result in an increased frequency of DGC-performing individuals in the population. Groenewald et al (2014) reported 100% prevalence of DGC for the mesic grasshopper Paracinema tricolor (Orthoptera: Acrididae) at 15°C. Importantly, insect metabolic rate and DGC are temperature dependent (Contreras and Bradley, 2010), and therefore DGC prevalence is expected to change with experimental temperature.…”

“…Moreover, earlier studies provided the first experimental challenge to the hygric hypothesis, showing that DGC is abolished in dehydrated insects when body water conservation is most essential Quinlan and Hadley, 1993). A more recent study showed that neither acclimation to dehydrating conditions nor acute exposure to low humidity resulted in shorter burst or longer interburst duration in grasshoppers (Orthoptera, Acrididae) (Groenewald et al, 2014).…”

“…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.…”