Surviving the winter

1 Surviving the winter

1.4 Strategy 2: dormancy in winter (‘opt out’)

1.4.1 Deciduous trees

During the winter months, a combination of factors, including lower temperatures, reduced light intensity and shorter days, means that plants can only photosynthesise at a slow rate and for restricted periods. As a result, photosynthesis cannot produce energy as fast as respiration expends it. In addition, water is often in short supply because of freezing, and so plants that do not have adaptations to conserve water, as conifers do, would lose water. Deciduous trees avoid these problems in winter by dropping all their leaves and shutting off photosynthesis. Before they do so, they dismantle the photosynthetic apparatus in their leaves and withdraw many of the constituents to their branches, trunks and roots.

Thus, in the autumn, sugars, amino acids and such minerals as nitrogen, phosphorus and potassium are transported from the leaves to woody tissues. Chlorophyll is broken down and the products are also withdrawn from the leaves. It is this process that causes leaves to change colour in the autumn. The breakdown of chlorophyll leaves behind other pigments, such as orange carotenes and yellow xanthophylls, which are normally hidden by the green chlorophyll. Once as many nutrients as possible have been withdrawn from a leaf, an abscission zone forms where the leaf stalk (petiole) meets the stem (Figure 1.12). Here the vessels that supply water and nutrients to the leaf are closed off and the leaf detaches, leaving a protective covering of cork over the scar. Leaf abscission is controlled by a complex system of hormones, responding to lower temperatures and light intensity and to shorter day length.

Figure 1.12 A section through the base of the petiole of a maple (Acer sp.) leaf before abscission, viewed under the light microscope after staining. The abscission zone comprises a layer of cells where the leaf becomes detached and a protective layer which seals the exposed surface of the stem following abscission.

1.4.2 Winter storage in plants

Many plants that survive winter in a dormant state form storage organs below the ground which store nutrients during the winter, the rest of the plant withering away. Storage organs come in a variety of forms, including tap roots, bulbs, corms, rhizomes, root tubers and stem tubers (Figure 1.13). In the carrot, the root is greatly enlarged into a fleshy tap root; the bulbs of onions are modified leaves; crocus corms, iris rhizomes and dahlia tubers are modified stems, and the tubers of potatoes are modified tips of underground stems.

Figure 1.13 Some examples of winter storage organs in plants: (a) tap root of carrot (Daucus carota, subsp. sativus); (b) bulb of onion (Allium sp.); (c) corm of crocus (Crocus sp.); (d) rhizome of iris (Iris sp.); (e) root tuber of dahlia (Dahlia sp.); (f) stem tuber of potato (Solanum tuberosum).

Unlike animals, few plants store energy reserves as fats (lipids). Those that do, generally store fats in seeds or fruits, a good example of the latter being the avocado (Persea americana). Storage in root organs is generally in the form of starch. Because they bind water, carbohydrates prevent desiccation of the storage organ and also reduce its freezing point, acting as ‘antifreeze’. Plant storage organs provide ready-made larders for those herbivores that remain active in winter.

The root of a carrot serves as a storage organ, enabling the plant to complete its two-year life cycle. The storage organs of many plants are, however, also a means of asexual or vegetative reproduction. For example, the rhizomes of irises grow and branch and, as older parts of a rhizome die, two or more new plants are formed from the parts that are left. The tubers of a potato plant can each grow into a new plant and the bulbs of such plants as onions and daffodils (Narcissus sp.) divide to produce new bulbs and thus new plants.

1.4.3 Freeze tolerance in ectothermic vertebrates

In Britain, the vertebrate class Amphibia is represented by frogs, toads and newts. Amphibians are ectotherms, meaning that they are unable to generate large quantities of heat within their bodies, so their body temperature is close to that of their surroundings. The majority of amphibian species avoid the lethal consequences of being frozen, by digging their way under a large object, such as a rock, or deep into the soil, below the level that is penetrated by frost. There are some species, however, that have evolved a physiological response to very cold weather that enables them to survive the winter on or close to the ground surface. Examples include the American wood frog (Rana sylvatica) and the Asian salamander (Hynobius kyserlingi), both of which have distributions that extend far north of the Arctic circle. What they do is to infuse their tissues with antifreeze.

In the wood frog, the onset of cold causes the animal to become immobile. As the temperature falls below 0°C, water in its toes begins to freeze. Within 10–15 minutes of freezing, glycogen stored in the liver is converted into soluble glucose which is released into the bloodstream, whence it finds its way into the cells and the extracellular spaces (Figure 1.14). The dissolved glucose lowers the freezing point of water, as antifreeze does in a car's radiator, preventing the formation of ice crystals and any consequent movement of water out of living cells.

Figure 1.14 (a) Changes in the concentration of glucose in various organs of the wood frog (Rana sylvatica) over 72 hours of freezing at −2.5°C in the laboratory. (b) The corresponding depletion of liver glycogen reserves. Note that the horizontal axes are non-linear. Data from Pinder et al. (1992).

Whereas the wood frog uses glucose as an antifreeze, the Asian salamander and the grey treefrog (Hyla versicolor) use glycerol, suggesting that this adaptation may have evolved independently in a number of amphibian species. Freeze tolerance allows these amphibians to survive freezing conditions for one or two weeks. It is not their only adaptation for surviving the winter; in the wood frog, for example, breathing ceases and the heart stops beating at very low temperatures.

Some ectothermic vertebrates rely on supercooling to survive short periods of cold temperature (see Section 1.2.1). For example, the spring lizard (Sceloporus jarrovi), living in the Arizona desert, survives very cold nights by supercooling. This strategy is risky, however, and many lizards die as a result of becoming frozen. Allowing its tissues to supercool is not a viable option for a frog or salamander; living in damp places, they are virtually certain to be in contact with ice crystals which act as nucleation points.

As well as enabling them to survive frosty conditions, the capacity to tolerate extreme cold confers other advantages on some amphibians. Many breed in temporary ponds that dry up early in the spring or summer, making it advantageous for breeding adults to migrate to ponds as early as possible in the spring. Early breeding maximises the time available for the aquatic egg and larval stages to be completed before a pond dries up. Some species, such as the American blue-spotted salamander (Ambystoma laterale) migrate to breeding ponds while snow is still on the ground, giving them an advantage over other salamander species that do not start to breed until the weather is warm.

1.4.4 Hibernation in mammals

Many animals become inactive for periods of varying duration during the winter and there is a diversity of terms used to describe this state, including: sleep, torpor, dormancy, lethargy and hibernation. The word hibernation is often used loosely to refer to general inactivity but, in biology, it refers to a specific phenomenon, sometimes called ‘true hibernation’. Hibernation is defined as the condition of passing the winter in a resting state of deep sleep, during which metabolic rate and body temperature drop considerably. It occurs only in certain mammals and one bird species, the poorwill (Phalaenoptilus nuttallii), a North American relative of the nightjar.

The phenomenon of hibernation is one reason why the term homeothermy is going out of fashion, to be replaced by endothermy, because maintaining a stable body temperature is the very opposite of what hibernators do. Instead, body temperature falls, from around 38°C, to about 1°C above ambient temperature, which is often close to 0°C. At the same time, a hibernator's metabolic rate falls to as little as 1% of its normal value. The heartbeat becomes slow and irregular and breathing rate also slows.

Hibernation is an active process, that is, it is a state which animals enter into, not in response to immediate external conditions, but to internal stimuli. Some species are remarkably precise and predictable. For example, the arctic ground squirrel (Spermophilus undulatus) enters hibernation between 5 and 12 October and emerges between 20 and 22 April, regardless of the weather on those dates. This behaviour is in contrast to other winter states such as torpor or lethargy which are immediate responses to current conditions. Brown and black bears, for example, are lethargic during very cold periods but are otherwise active in the winter. A feature of hibernation that distinguishes it from other kinds of winter inactivity is that hibernators can arouse themselves spontaneously and are not dependent on external conditions, such as warm temperatures, to do so. The arctic ground squirrel is described as an obligate hibernator because it hibernates every winter. There are some mammals that are categorised as facultative hibernators, entering hibernation in response to very cold weather and poor food supply. The North American pocket mouse (Perognathus californicus) is a facultative hibernator.

True hibernation only occurs in relatively small mammals, though not all small mammals living in temperate habitats hibernate in winter, as we have seen. The largest mammal to hibernate is the marmot, which weighs about 5 kg. There are several reasons why larger mammals do not hibernate. Firstly, they would warm up too slowly and therefore use too much energy. Secondly, they have a smaller surface area to volume ratio and so can conserve body heat better than smaller species. Finally, they are better able to carry a thick coat (Section 1.3.2) and sufficient adipose tissue to last through the winter. Hibernators are mainly found in the orders Rodentia, Chiroptera (bats) and Insectivora. The hedgehog (Erinaceus europaeus) is an example of a hibernating insectivore; in Britain, it hibernates from October/November to March/April. Note that although hedgehogs are in the order Insectivora they do not just eat insects!

The physiological features that are characteristic of hibernation are not maintained throughout the winter. Rather, the animal wakes up at intervals, its temperature and metabolic rate increasing to near-normal levels (Figure 1.15). The function of this periodic arousal is not wholly clear. Some species, such as the chipmunks (genus Tamias) eat from stored food reserves during arousal periods, but many others do not. Most species urinate and defecate, move about and change their position, suggesting that arousal provides an opportunity for various essential physiological processes to be performed and to prevent the animal becoming moribund. From detailed measurements of Richardson's ground squirrel (Spermophilus richardsonii) in the laboratory, it has been calculated that, during the relatively brief periods of arousal (Figure 1.15), an individual expends 83% of all the energy that it uses up during the entire hibernation period.

Figure 1.15 Record of body temperature from September to March for a Richardson's ground squirrel. Data from Pough et al. (1996).

Hibernation requires internal energy reserves in the form of adipose tissue and hibernators typically feed intensively prior to winter, building up their fat stores. Some species, such as the edible dormouse (Glis glis), switch to a carbohydrate- and lipid-rich diet, e.g. seeds, at this time. A characteristic of hibernating mammals is that they possess larger quantities of a particular kind of adipose tissue called brown adipose tissue (BAT). This tissue gets its name from its dark colour, which is due to the larger numbers of blood capillaries that permeates it and the high concentration of mitochondria within the cells. BAT is rich in mitochondria with special properties that enable it to oxidise fatty acids and/or glucose to produce heat very rapidly. BAT deposits are found around some internal organs and between the shoulder-blades of hibernators and their function is to generate body heat very rapidly, especially during periods of arousal.

Hibernation might seem to be a safe, and rather agreeable way to spend the winter but, for some species, it is fraught with danger. For Belding's ground squirrels (Spermophilus beldingi) living at high altitude in Tioga Pass, California, hibernation lasts 7–8 months. Two-thirds of all juveniles, hibernating for the first time, and one-third of adult animals die during hibernation. Some die because their fat reserves run out before the end of hibernation; others are dug up and eaten by predators.

Some mammals spend the winter in groups, huddled together during periods of dormancy, and so conserve body heat. North American raccoons (Procyon lotor), for example, spend dormant periods in communal dens. Many species of bats hibernate communally. During hibernation, the body temperature of some bats can fall below 0°C. In the autumn, they build up fat reserves that represent as much as a third of their total mass. During the winter, bats arouse themselves from hibernation to excrete and sometimes also to move to a new roost. A critical factor for hibernating bats is that roosting sites have high humidity and some populations have to migrate quite large distances to find suitable places, such as caves and hollow trees.

For some mammals, hibernation is closely associated with other important activities, notably reproduction and dispersal. Consequently, energy reserves may have to support more than one activity. For example, brown bears living at northern latitudes mate in the autumn and give birth to their cubs during winter lethargy. Edible dormice and some bats mate immediately after the end of hibernation. (In some species of bats, males wake up first and mate with the females before they have woken up!) The link between what animals do in winter and their reproductive cycles was discussed in Section 1.2.3.

Natal dispersal is the permanent departure of an individual from its place of birth, usually at the end of the breeding season. It is an important part of the life history of many animals, especially mammals, and tends to be sexually dimorphic, males dispersing further than females. Natal dispersal is potentially both hazardous and energetically expensive; dispersing animals tend to be vulnerable to predators and, being on the move, have little time to feed. Dispersal therefore requires internal energy reserves in the form of fat, the very same reserves that they later need to survive the winter. There may thus be a trade-off in the allocation of energy reserves to dispersal and to hibernation.

Scott Nunes of Michigan State University has studied dispersal and hibernation in Belding's ground squirrels in a locality where hibernation lasts for eight to nine months of the year. Young males typically disperse after the summer breeding season but show much variation in the extent to which they do so, with fatter males being more likely to move out of the natal area. In years when breeding is delayed, dispersal is inhibited; instead, young males remain near the natal area, building up their fat reserves prior to hibernation. The findings of this study are summarised in Figure 1.16.

Figure 1.16 A graphical summary of the control of dispersal in male Belding's ground squirrels. See text for explanation.

If young males are ready to disperse early (date A in Figure 1.16), they leave with relatively small fat reserves. In this situation, they have time to travel further to a new area and then build up fat reserves before hibernation. If dispersal is delayed (dates B and C), males do not disperse unless they have built up a threshold level of fat reserves; the value of this threshold increases as winter approaches. In other words, the trade-off between dispersal and hibernation is resolved by hibernation suppressing dispersal, unless an animal exceeds a certain fat level. After date C, dispersal is inhibited regardless of the size of the fat reserves.

Summary of Section 1.4

1. Deciduous trees avoid the problems of winter by shedding their leaves.
2. Plants can store nutrients over winter in a variety of structures.
3. Amphibians have evolved behavioural responses (e.g. burying themselves) and physiological responses (e.g. different types of antifreeze in the body fluids) to winter.
4. Hibernation occurs only in certain small mammal species and one species of bird and is accompanied by marked physiological and behavioural changes.
5. Prior to hibernation, animals build up their fat reserves and frequently possess larger amounts of brown adipose tissue than non-hibernators.
6. There may be a trade-off between hibernation and dispersal in some animals.