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

Authors: HAYWARD, SCOTT - LIVERPOOL UNIVERSITY; Rinehart, Joseph - Joe; SANDRO, LUKE - MIAMI UNIV, OXFORD, OH; LEE, RICHARD - MIAMI UNIV, OXFORD, OH; DENLINGER, DAVID - OHIO ST UNIV, COLUMBUS

Submitted to: Experimental Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/11/2007
Publication Date: 3/1/2007
Citation: Hayward, S.A., Rinehart, J.P., Sandro, L.H., Lee, R.E., Denlinger, D.L. 2007. Slow dehydration promotes desiccation and freeze tolerance in the Antarctic midge Belgica antarctica. The Journal of Experimental Biology. 210(5):836-844.

Interpretive Summary: Antarctica, being the coldest and driest continent on earth, contains some of the earth’s most inhospitable environments. Although an abundance of animals have adapted to life in the sea in this part of the world, few animals have adapted to living on the continent itself. One exception is the midge Belgica antarctica, which at ¼ of an inch long, is Antarctica’s largest free-living, year-round inhabitant. Previously, our research team has studied the cold tolerance of this insect. However, dry conditions are equally important, especially because water, in the form of ice, is biologically inaccessible for much of the year. This study investigates how this insect responds to dry conditions. We have found that at a humidity as high as 98%, this insect will lose water from its body. While easily losing water does not at first seem like a good adaptation for survival in Antarctica, our data suggests that it may actually be beneficial to this species. First of all, this insect is highly tolerant of dehydration (water loss), with half of the individuals surviving a loss of 75% of body water (in comparison, a 20% loss is usually considered deadly to humans). Secondly slow dehydration, such as the rate of water loss at 98% humidity, allows for greater survival than rapid dehydration. Finally, there is a link between cold survival and dehydration. Dehydrated insects are more likely to survive cold exposure than their fully hydrated counterparts. Hence, this unique management of body water is yet another means by which this species has adapted to the harsh Antarctic continent.

Technical 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. Survival rates were further increased when rehydration was performed at 100%•RH, rather than by direct contact with water. 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.