Frozen for Winter

As winter turns to spring and the temperature begins to rise, we thankfully put away our warm winter clothes and look forward to perhaps a little less rain. Out there beyond the double-glazing, in the garden and in the countryside, we are vaguely aware that animals are also stirring, but few of us realise the extraordinary lengths to which other creatures are forced to go in order to survive those long cold foodless winter months.

Picture a good night’s sleep after a hearty meal. Picture waking at breakfast time,  the hunger that you feel, and the gnawing hunger that it becomes by lunchtime if you couldn’t be bothered to eat breakfast. Imagine that hunger after three whole months of sleeping outside in the winter cold. Clearly, there is more to winter survival than mere sleep.

In fact, hibernation is so different from sleep that hibernating mammals have to wake up every few weeks just so that they can get some normal sleep, otherwise they suffer from sleep deprivation. During normal sleep, brain activity continues. In deep hibernation, an EEG reading is essentially flat; in this condition a human would be considered to be clinically dead.

Hibernation is not a response to cold weather as such. The point is not to survive the cold, but to cope with freezing temperatures when you have no food. Hibernation is not even triggered by cold weather; it is an instinctive programmed annual event triggered by the changes of the seasons, and requires some preparation.

In the months before hibernation, mammals build up stores of a special brown fat with remarkable properties. Normal fat, as found in the spare tyre of middle-age spread, is used for the long term storage of chemical energy. When an animal is hungry enough (or the couch potato embarks on yet another diet), this fat is used as fuel and is chemically ‘burnt’ to provide energy. Brown fat, on the other hand, is processed by a different chemical pathway. It is stored wrapped around critical organs such as the heart and central nervous system, and when it is processed its stored energy is given off as genuine heat. When the animal needs to warm up again, it is this brown fat that does the job.

All mammals that truly hibernate are small, with every point of the body close to the exterior, and so the core can cool or warm rapidly in just a few hours. Larger animals are just too big to do this in a reasonable time, as not only would some organs remain chilled while others were already fully functioning, but some of the larger structures such as the liver would suffer from uneven warming across the organ itself. While it is true that brown bears spend much of the winter dormant, their body temperature only drops by a few degrees and they never really hibernate. On the other hand, most small mammals drop their core temperature right down to just above freezing.

In terms of survival without food, hibernation at this level is an excellent investment. If you consider that every 1 degree fall in core temperature from the normal 30 degrees or so represents a halving of the energy needed to survive, and that energy can only be obtained from ever-scarcer food, it is clear that hibernation is worth it.

However, freezing point is the limit beyond which most mammals cannot go. A high percentage of any animal’s body weight is water, much of it inside soft vulnerable cells. If this water freezes, the sharp spiky ice crystals wreak havoc as they grew irresistibly through the soft cell membranes. Any gardener knows the devastating effect that an unexpected late frost can have on unprotected young garden plants, reducing them almost overnight to an evil-smelling brown mush.

At least one mammal has managed to breach this limit. The sik-sik, a small squirrel in northern Alaska, has recently been found hibernating in burrow temperatures of down to -25 degrees centigrade. In order to keep warm in these extreme conditions it has developed some novel biochemical tricks, but in addition these squirrels can cool to the lowest body temperature ever measured for a mammal, -3 degrees centigrade.

It does this by a technique known as supercooling. In cooling water, ice crystals don’t just appear at random, they need to form around small particles or impurities. If the water is extremely pure, or if suitable seed particles can be removed or shielded in some way, it is possible to cool water well below zero without it freezing. The squirrel somehow removes all suitable seed sites from its blood before hibernating – just how it does this is still a mystery.

The technique is very risky. If a single ice crystal forms in supercooled water, it can itself act as a seeding site for other crystals, sparking a runaway reaction in which the entire body of water freezes solid in an instant. If any solid particle makes contact with the squirrel’s blood – for instance an icicle grows in the burrow and breaks the skin – then the entire animal freezes catastrophically and dies.

The sik-sik is a special case. Most mammals are not subjected to such extremes of low temperature and sparse food, and are quite able to survive by getting very fat and then keeping their body temperatures just above the dangerous freezing point until the spring thaw brings new food. However, by far the greater part of the animal population consists of so-called ‘cold-blooded’ creatures, incapable of regulating their body temperatures at all. Insects, fish, reptiles and amphibians all have no choice but to accept that their bodies will be at the same temperature as the outside world. This is the reason that many insects only live for a single season, relying on their carefully hidden or buried eggs or pupae to carry on the species. Other insects overwinter as aquatic larvae, where alongside hibernating frogs and turtles they are safe unless the body of water freezes completely. On land, many toads and snakes dig down below the frost line.

Many of these animals make use of the sik-sik’s supercooling trick. Many more flood their bodily fluids with antifreeze – often the same ethylene glycol that we put into our car radiators –  sometimes with astounding effect. Arctic and Antarctic fish regularly swim about in water that is several degrees below zero, and some insects live an active life at -15 degrees beneath the Arctic snow pack.

This still is not enough for some insects; the larvae of the spruce budworm can survive temperatures as low as -30 centigrade, and caterpillars of the gall moth have been found with 40 percent of their bodily fluids replaced by antifreeze – that’s 19 percent of their bodyweight – ensuring their survival down to -38 centigrade.

The real overwintering prize, though, has got to go to those animals – various frogs, insects, and freshwater turtles – that actually allow themselves to freeze solid for the winter, only thawing out in the Spring. Once frozen, all their internal organs are completely solid, making essential movements such as heartbeats and breathing impossible. The spark of life is maintained by individual cells all through the winter using whatever resources they have within themselves, as no new food or oxygen can arrive until the animal thaws out again.

Animals that freeze do not try to cut down on seed particles in their body fluids. In fact, they flood the blood with special proteins that actually encourage ice formation, relying on the sheer numbers of seeds to form a great many small ice crystals rather than the more damaging large ones. Since small ice crystals are inherently unstable, and tend to merge together over time into larger crystals, many of these animals also contain large quantities of antifreeze in an attempt to stabilise the ice growth.

The story does not end there. The fluids both inside cells and in the spaces between them consist of a number of salts, sugars and proteins dissolved in water. It is critical to life that the relative concentration of the fluids inside and outside the cells remains constant, a balance that is usually carefully maintained by the living cell membrane.

Ice is pure frozen water, effectively distilled from the impure water from which it formed, and when the freezing process begins, any chemicals that were dissolved in the water just have to get out of the way. In animal tissue it is the free fluid outside of the actual cells that begins to freeze first, and as the first water turns into ice, the substances that were dissolved in it are forced to move out into the remaining unfrozen liquid.

As ever more water freezes, more dissolved chemicals escape into whatever fluid is left, so that the unfortunate cell, as yet unfrozen itself, becomes surrounded by sharp ice crystals and intensely concentrated fluid. High concentrations of anything are potentially toxic, but there is a more serious problem.

The critical balance between the fluids inside and outside a cell is maintained by the cell membrane, a marvellous structure full of pumps and filters that continually shifts chemicals and solvents one way or the other in an intricate dance. As the vital balance between the concentrated liquid outside the cell and the more normal liquid inside it becomes upset, the living cell membrane attempts to dilute the poisonous sea outside with pure water from inside. The moment this water gets outside the cell wall it swiftly freezes and joins the legions of encroaching ice.

The cell can only take so much of this. The interior fluid too becomes more and more concentrated, and as the water leaves, the cell shrinks, squeezing the essential structures within it. The process only stops when the external fluid is so concentrated that it can no longer freeze, and usually by this point the cell of a normal animal is already dead.

The cell membranes of freeze-tolerant animals, on the other hand, are beefed up with special proteins that protect the cell wall as it wrinkles up during shrinkage. A normal mammal can tolerate the freezing of around 2% of its body water before it dies. Typically, freeze-tolerant animals can survive with up to 65% of their body water frozen into ice.

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