The role of the gut in insect chilling injury: cold-induced disruption of osmoregulation in the fall field cricket,Gryllus pennsylvanicus

Abstract

SUMMARYTo predict the effects of changing climates on insect distribution and abundance, a clear understanding of the mechanisms that underlie critical thermal limits is required. In insects, the loss of muscle function and onset of cold-induced injury has previously been correlated with a loss of muscle resting potential. To determine the cause of this loss of function, we measured the effects of cold exposure on ion and water homeostasis in muscle tissue, hemolymph and the alimentary canal of the fall field cricket, Gryllus pennsylvanicus, during an exposure to 0°C that caused chilling injury and death. Low temperature exposure had little effect on muscle osmotic balance but it dissipated muscle ion equilibrium potentials through interactions between the hemolymph and gut. Hemolymph volume declined by 84% during cold exposure whereas gut water content rose in a comparable manner. This rise in water content was driven by a failure to maintain osmotic equilibrium across the gut wall, which resulted in considerable migration of Na + , Ca 2+ and Mg 2+ into the alimentary canal during cold exposure. This loss of homeostasis is likely to be a primary mechanism driving the cold-induced loss of muscle excitability and progression of chilling injury in chill-susceptible insect species.Supplementary material available online at

Reestablishment of ion homeostasis during chill-coma recovery in the cricketGryllus pennsylvanicus

“…We tracked ion and water content in hemolymph, muscle, and the gut during recovery from a standardized 24-h cold exposure. As previously reported (25), exposure to 0°C for 24 h led to a decrease in hemolymph [Na + ] (P = 0.017) but did not alter muscle Na + equilibrium potentials (E Na ; P = 0.582; Fig. 2B), possibly due to a concurrent decrease in intracellular Na + concentration (Fig.…”

“…1B and Table S1). This second, variable phase beyond 24 h corresponds with the time-course over which G. pennsylvanicus begin to accumulate irreversible chilling injury, which manifests as a permanent loss of muscle control, and eventual death (25). Thus, the increase in the mean and variance of CCR beyond 24 h of cold exposure likely results from accumulated chilling injury that impairs coordinated movement but does not affect the ability to move isolated groups of muscles.…”

“…Gryllus pennsylvanicus were maintained in a laboratory colony as previously described (25). All experiments were completed on gravid adult females, approximately 3 wk following final molt.…”

“…The onset of chill-coma is caused by an inability to maintain hemolymph osmotic homeostasis, leading to electrophysiological failure of the neuromuscular system (24,25). In the fall field cricket (Gryllus pennsylvanicus), a cold-induced redistribution of Na + and water from the hemolymph to the gut during chill-coma elevates hemolymph K + concentration, depolarizing muscle K + equilibrium potentials (E K ) (25).…”

“…In the fall field cricket (Gryllus pennsylvanicus), a cold-induced redistribution of Na + and water from the hemolymph to the gut during chill-coma elevates hemolymph K + concentration, depolarizing muscle K + equilibrium potentials (E K ) (25). Once the muscle depolarizes beyond a threshold membrane potential, contraction and/or relaxation are no longer possible and the insect is paralyzed (26).…”