Winter World_ The Ingenuity of Animal Survival - Bernd Heinrich [78]
Goldenrod gall, showing cross section with gall fly larva (center) and two galls on one stalk, both excavated by downy woodpecker (right).
In the goldenrod fly, as in the previously discussed Arctiid moths, only the larval stage is physiologically specialized to overwinter, and the insect’s life cycle of one generation per year is adjusted to bring the larval stage to winter. After passing through the winter the larvae pupate and then emerge as adult flies in time to parasitize tender goldenrod shoots. By late summer the goldenrod, the gall, and the larva have stopped growing and the larva then chews an escape tunnel from the center of the gall all the way to, but not through, the outermost edge. Retreating back into the center of the tough woody gall, it spends the winter there, in hibernation. That the larva makes the escape hatch when it does is essential, because the adult gall fly does not have chewing mouth-parts and it would otherwise remain entombed within the gall. Having prepared both an overwintering site and a means for the fly emerging in the spring to escape from it, the larva next prepares physiologically for meeting the winter cold. Northern populations of the fly have different responses than the southern.
Northern Eurosta larvae prepare for winter by producing both glycerol (an alcohol) and sorbitol (a sugar) in response to lowered temperature in the fall. The lower the temperature, the more glycerol and sorbitol they produce and the lower the freezing point of their blood. But their frost-hardiness doesn’t end there. It involves far more complex and sometimes counterintuitive mechanisms, all acting in concert, that not all readers will likely want to follow. This includes, for example, the paradox that the northern larvae produce and release a protein into their blood that promotes freezing. In effect, the protein mimics ice crystals by providing nucleation sites for ice crystal formation. It thereby prevents the animal from achieving supercooling. By preventing supercooling, the protein causes the larvae to freeze earlier, already at higher temperatures than they would otherwise.
How can the apparent promotion of freezing aid in winter survival, even as the animals produce compounds with antifreeze properties? The answer is complex, and elegant. It relates to the fact that very low temperatures may be encountered in the northern larvae populations, and antifreeze alone would then be insufficient to guarantee absence of ice formation. With no guarantee of avoiding freezing, the animals have then found a way to survive it. Their antifreeze glycerol serves a dual function. It lowers the freezing point, thus reducing the probability of freezing, but when or if freezing does occur, then the glycerol acts to reduce the damage caused by ice crystals. Indeed, glycerol is found in both freeze-intolerant and freeze-tolerant species, having a different function in each.
Freezing-avoidance by supercooling is of course also potentially adaptive. But only at consistently modest low temperatures. At even occasionally very low environmental temperatures, when freezing is highly possible, if not inevitable, then supercooling is dangerous because it could cause instant freezing and sure death. To understand why, we need to keep two things in mind. First, supercooled larvae, if seeded with an ice crystal, would freeze nearly instantly (the exact speed, in seconds, would depend on the amount of supercooling). Second, although some insects can indeed survive being frozen, they can do so only if that freezing proceeds slowly. Any insect—or any animal—that freezes instantly, as when supercooled, then also dies instantly.
Rate of freezing is important for cell survival because of a compartmentalization of ice crystals that relates ultimately to dehydration. During slow freezing the fluid surrounding the cells freezes first, because it is more dilute than the fluid within the cells. As ice crystals form