Interactions of water, ice nucleators and desiccation in invertebrate cold survival

Abstract

Abstract. Four case studies are used to examine the relationships of water, ice nucleators and desiccation in the cold survival of invertebrates and the viability of frozen plant material: the freeze intolerant Antarctic springtail Cryptopygus antarcticus (Willem) (Collembola, Isotomidae), the freeze tolerant larvae of the fly Heleomyza borealis Boh. (Diptera: Heleomyzidae), the freeze intol erant Arctic springtail Onychiurus arcticus (Tullberg) (Collembola, Onychiuridae) and meristems of the currant Ribes ciliatum Humb. & Bonpl.(Grossulariaceae) from Mexico. Prevention of ice nucleation, lowering the water content by removal of osmotically active (freezable) water are critical features of the different cold survival strategies of the three species of invertebrates. In C. antarc ticus, which desiccates rapidly by losing water via the cuticle to the atmosphere, the number of ice nucleators (and their activity) increases with lowered ambient temperature. During prolonged cold exposure ice nucleators are masked, but re-activated rapidly by water uptake in this species. Larval H. borealis do not readily desiccate and conserve their body water, 20-25% of it being bound (osmotically inactive). Experiments showed that a high proportion (c. 80%) of slowly cooled larvae survived exposure to -60°C. By comparison O. arcticus is able to sustain up to 40% loss of its body water and desiccation lowers its supercooling point to promote over winter survival. Dehydration leading to partial vitrification of currant (R. ciliatum) meristems improves their viability after cryopreservation in liquid nitrogen. From this comparison of four biological systems, it is concluded that the role of water and its activity at sub-zero temperatures are fundamental to the survival of freezing conditions by all the species studied. Although similar features exist in the four systems, no common basic mechanism was found.

A case study of Heleomyzidae (Diptera) recorded on snow in Poland with a review of their winter activity in Europe

“…The lowest supercooling point was reported for the chironomid Diamesa mendotae Muttkowski (-21.6°C) (Bouchard et al, 2006). It is noteworthy that some fl ies can survive even long, severe and snowy winters as immature stages: for example, larvae of Heleomyza borealis, a snow-active fl y especially widely distributed in the Arctic, can survive temperatures as low as -60°C and need a lower than -15°C temperature stimulus and thereafter warmer period to pupate (Block, 2002). Despite the known low temperature preferences of the species of this family, snow-recorded Heleomyzidae have been intensively studied only by Hågvar & Greve (2003).…”

Cold tolerance in terrestrial invertebrates inhabiting subterranean habitats

“…2000; Block, 2002;Block & Zettel, 2003;Ansart & Vernon, 2003;Sinclair et al, 2003;Hodkova & Hodek, 2004;Danks, 2006;Lagerspetz & Vainio, 2006;Hawes & Bale, 2007;Bowler & Terblanche, 2008;MacMillan & Sinclair, 2011;Vesala & Hoikkala, 2011). The stepwise 1°C-graded arrangement of our experiment does not allow precise determination of the LLTs; the real values may be, on average, about 0.5°C higher.…”

“…In practice, some aquatic (Hervant & Mathieu, 1997;Issartel, 2007;Colson-Proch et al, 2009) and terrestrial troglobionts (Peck, 1974;Latella et al, 2008;Lencioni et al, 2010) clearly show cold resistance. On the other hand, most Antarctic and Alpine species, which in their microhabitats are thermally buffered at above-zero temperatures, are intolerant to freezing (e.g., Zettel, 2000;Block, 2002;Elster & Benson 2004;Lipovšek et al, 2004;Novak et al, 2004).…”

Insect adaptations to cold and changing environments

“…Water bound more or less tightly to cellular constituents has been termed "unfrozen water" or "osmotically inactive water" (also, less usefully, "unfreezable water" or "bound water"). Wolfe et al (2002) pointed out that the amount of unfrozen water may exceed the potentially "unfreezable" amount because equilibrium is not reached over normal time frames at low temperatures; see Block (2002Block ( , 2003 for further discussion. Unfrozen water comprises 10%-30% of the total water in different species (Storey and Storey 1988;Block 1996), and typically the proportion that will not freeze increases in preparation for winter (Storey et al 1981;Storey and Storey 1988).…”