Slow dehydration promotes desiccation and freeze tolerance in the Antarctic midge Belgica antarctica

Abstract

Adaptations to low moisture availability are arguably as important as cold resistance for polar terrestrial invertebrates, especially because water, in the form of ice, is biologically inaccessible for much of the year. Desiccation responses under ecologically realistic soil humidity conditions--those close to the wilting points of plants [98.9% relative humidity (RH)]--have not previously been examined in polar insect species. In the current study we show that, when desiccated at 98.2% RH, larvae of the Antarctic midge Belgica antarctica are more tolerant of dehydration than larvae desiccated at lower humidities (75% RH), and develop an increased tolerance to freezing. The slow rate of desiccation at this high RH enabled more than 50% of larvae to survive the loss of >75% of their osmotically active water (OAW). Survival rates were further increased when rehydration was performed at 100% RH, rather than by direct contact with water. Two days at 98.2% RH resulted in a approximately 30% loss of OAW, and dramatically increased the freeze tolerance of larvae to -10 and -15 degrees C. The supercooling point of animals was not significantly altered by this desiccation treatment, and all larvae were frozen at -10 degrees C. This is the first evidence of desiccation increasing the freeze tolerance of a polar terrestrial arthropod. Maximum water loss and body fluid osmolality were recorded after 5 days at 98.2% RH, but osmolality values returned to predesiccated levels following just 1 h of rehydration in water, well before all the water lost through desiccation had been replenished. This suggests active removal of osmolytes from the extracellular fluids during the desiccation process, presumably to intracellular compartments. Heat-shock proteins appear not to contribute to the desiccation tolerance we observed in B. antarctica. Instead, we suggest that metabolite synthesis and membrane phospholipid adaptation are likely to be the underpinning physiological mechanisms enhancing desiccation and cold tolerance in this species.