dormancy

/dawr"meuhn see/, n.

the state of being dormant.

[1780-90; DORM(ANT) + -ANCY]

* * *

▪ biology

Introduction

      state of reduced metabolic activity adopted by many organisms under conditions of environmental stress or, often, as in winter, when such stressful (stress) conditions are likely to appear.

      There are few environments in which organisms are not subject to some kind of stress. Some animals migrate vast distances to avoid unfavourable situations; others reduce environmental stresses by modifying their behaviour and the habitats (immediate surroundings) that they occupy. Arctic lemmings, for example, are able to avoid severe winter weather by confining their life in winter to activities beneath the snow cover. Still another mechanism (metabolism) used by some organisms to avoid stressful environmental conditions is that of dormancy, during which an organism conserves the amount of energy available to it and makes few demands on its environment. Most major groups of animals as well as plants have some representatives that can become dormant (hibernation). Periods of dormancy vary in length and in degree of metabolic reduction, ranging from only slightly lower metabolism during the periodic, short-duration dormancy of deep sleep to more extreme reductions for extended periods of time.

General observations

Value of dormancy

      In terms of evolution, dormancy seems to have evolved independently among a wide variety of living things, and the mechanisms for dormancy vary with the morphological and physiological makeup of each organism. For many plants and animals, dormancy has become an essential part of the life cycle, allowing an organism to pass through critical environmental stages in its life cycle with a minimal impact on the organism itself. When lakes, ponds, or rivers dry up, for example, aquatic organisms that can enter a period of dormancy survive, while others perish. Moreover, animals that can become dormant during the extreme cold of winter can extend their ranges into regions where animals incapable of dormancy cannot live. Dormancy also ensures that these animals will be free from competition during their periods of activity. Thus, dormancy is an adaptive mechanism that allows an organism to meet environmental stresses and to take advantage of environmental niches that otherwise would be untenable at certain times.

Causes of dormancy

      The dormant state that is induced in an organism during periods of environmental stress may be caused by a number of variables. Those of major importance in contributing to the onset of dormancy include changes in temperature and photoperiod (photoperiodism) and the availability of food, water, oxygen, and carbon dioxide. In general, because organisms normally exist within a relatively narrow temperature range, temperatures above or below the limits of this range can induce dormancy in certain organisms. Temperature changes also affect such other environmental parameters as the availability of food, water, and oxygen, thus providing further stimuli for dormancy. In Arctic regions, for example, certain animals become dormant during the winter months, when food is less abundant. In desert biomes, on the other hand, the summer months, which may be periods of reduced food availability, intense heat, or extreme aridity, stimulate some desert organisms to become dormant. The lack of water during summer periods of drought or winter periods of freezing, as well as annual changes in the duration and intensity of light, particularly at high latitudes, are other environmental factors that can induce dormant states.

      Under natural conditions, most of the environmental variables that influence dormancy are interrelated in a cyclical pattern that is either circadian or annual. Fluctuations in the major daily variables—light and temperature—can induce rhythmical changes in the metabolic activity of an organism; annual fluctuations in temperature and photoperiod can influence the availability of food and water. Concentrations of oxygen and carbon dioxide normally do not vary on a cyclical basis but as a result of habitat selection, such as burrowing in the mud, seeking a den, or other similar activities, in which the metabolic responses of the organism can alter the oxygen and carbon dioxide concentrations in its environment.

      In an attempt to determine the relative influence of environmental factors upon dormancy, they have been varied experimentally. Investigations indicate that an organism, after it has adapted to a sequence of cyclical rhythms, tends to maintain its adaptive behaviour even though the environmental stimulus that originally elicited such behaviour is no longer present. For example, the Arctic ground squirrel (whose winter period of dormancy is referred to as hibernation), when taken into the laboratory, supplied with adequate amounts of food and water, and exposed to constant temperature and light, exhibits periodic torpor (extreme sluggishness)—an innate behavioral pattern that operates independently of environmental cues. Other animals frequently will continue to respond as if they were exposed to the cyclical changes of their home environments after they are removed from their natural habitats.

Dormancy in protozoans (protozoan) and invertebrates

Cysts and cystlike structures

Protozoans

      Many parasitic and free-living protozoans (one-celled animals) exhibit a dormant stage by secreting a protective cyst. The stimulus for cyst formation in free-living protozoans may be temperature changes, pollution, or lack of food or water. Euglena, a protozoan that encysts to avoid environmental extremes, has two kinds of cysts. Apparently one is formed only to avoid stressful conditions; the other is formed for the same reason but also involves asexual reproduction, resulting in a cyst that may contain up to 32 daughter organisms, which emerge under proper environmental conditions.

      Free-living protozoans form cysts around themselves and avoid environmental extremes, but cysts are a part of the life cycle of parasitic protozoans. The causative agent of amebic dysentery, Entamoeba histolytica, is found in the intestine of infected individuals, in whom it forms cysts that pass to the outside in feces. When food or water containing cysts enters the digestive tract of another person, the amoebas are released from the cysts and infect the new host. Without encystment, which allows the organism to live in a dormant state in an unfavourable environment (e.g., water), amebic dysentery could be much more easily controlled. Protected by the cyst wall, however, the dormant contents of the cyst can survive for weeks. Although they are not particularly resistant to drying, the cysts of E. histolytica can withstand temperatures of up to 68° C (154° F) for five minutes. They are also resistant to certain chemicals.

Invertebrates

      Dormant cysts are formed during the life cycles of invertebrate parasites such as the oriental liver fluke (Clonorchis sinensis). The cyst stage of this organism develops in fish muscle; if the fish is eaten raw or undercooked, the encysted fluke is transferred to a new host. The encysted stage of the trichina worm (Trichinella spiralis), which causes trichinosis, is found in the muscle cells of hogs; it is also an invertebrate parasite in which the dormant stage is an essential part of the life cycle. When undercooked pork is eaten, the cyst wall is dissolved by digestive juices, and the worm is able to make its way into the tissues of a new host.

      The cystlike forms found in many other invertebrate groups are all dormant stages that preserve the species during times of environmental stress. All freshwater sponges (sponge) and some marine species survive cold or drought by forming gemmules within the body of the adult sponge. These structures, which are surrounded by a resistant covering, are released when the sponge dies and disintegrates. When conditions are appropriate, the cell mass escapes from the covering and forms a new sponge.

      Rotifers (rotifer) are microscopic aquatic animals that produce winter eggs (egg) with thick and resistant coverings similar to protozoan cysts; the eggs may remain dormant for long periods. They can survive drought or freezing and may be dispersed by wind or carried by animals. Thus, the cyst serves not only for survival of the egg under adverse conditions but also for dispersal. Some freshwater bryozoans develop disklike buds, or statoblasts, that are surrounded by a hard, chitinous (horny) shell. These statoblasts are the dormant structures that survive when the bryozoan dies in the fall or during a drought; they form a new bryozoan colony when favourable environmental conditions again prevail.

      Among mollusks (mollusk), land snails (land snail) remain largely dormant throughout the day, with the soft head and foot withdrawn into the shell. During periods of drought or cold, they retreat into their shells and secrete a membrane (the epiphragm) of mucus and lime that covers the opening of the shell and resists desiccation. Slugs (slug), on the other hand, bore into the ground and secrete a mucus mantle around themselves for protection during periods of unfavourable environmental conditions. Among the arthropods (arthropod), many freshwater forms develop dormant cystlike stages that resist desiccation and allow the species to survive unfavourable periods.

diapause in insects (insect)

      Many insects undergo periods of reduced metabolic activity called diapause. Diapause, which may occur during any stage of the life cycle—egg, nymph, larva, pupa, or adult—is usually characterized by a cessation of growth in the immature stages and a cessation of sexual activity in adults. In some insects, it is a reaction to unfavourable environmental conditions; in others, such as certain moths and butterflies, diapause is a necessary stage of the life cycle. The 17-year larval and pupal periods of the cicada are examples of diapause. This form of dormancy is particularly common among insects that live in arid desert areas, where during the dry and hot summers, the insects usually hide themselves in the soil at suitable depths or under any available protective objects.

      Insects may overwinter as egg, larva, nymph, pupa, or adult; because they can stand very low temperatures, few of these forms die if the winter temperatures are within their normal range. Even rather fragile forms, such as mosquitoes and butterflies, survive in sheltered, relatively dry places out of doors. Some butterflies even survive the winter in low shrubbery, where they may be completely covered by snow and ice for three or four months. Other insects prepare for winter by constructing nests or cocoons; still others seek suitable hiding places.

      Among some insect species, diapause lasts only until favourable environmental conditions return, after which the insect resumes its normal activities. In other species, favourable environmental conditions alone do not break the diapause; some other stimulus, such as cold or food, is necessary. The eggs of the mosquito Aedes vexans, for example, remain in diapause until the damp soil on which the eggs are laid is flooded to form a pool suitable for the larvae. The eggs of another mosquito, Aedes canadensis, are laid in the same soil as those of Aedes vexans, but they will not hatch until they have been subjected to cold. Thus, when both species lay their eggs together in early summer, those of Aedes vexans hatch in pools formed by late summer rains, but those of Aedes canadensis overwinter and hatch in the spring rain pools. Not only are certain conditions required to break diapause but in some species (e.g., certain cutworms) a specific length of time must elapse before the stimuli are effective.

      The onset of diapause depends upon a combination of environmental factors operating on the regulatory mechanisms—i.e., nervous and endocrine systems (endocrine system)—of the insect. Photoperiod and temperature influence the endocrine function of the brain, which synthesizes and secretes a substance ( hormone) that controls other endocrine organs, specifically the prothoracic glands. Under the stimulation of the brain hormone, the prothoracic glands secrete a hormone called ecdysone. When stimulation by the brain hormone ceases, ecdysone is no longer secreted, and, in its absence, all insect growth and metamorphosis are halted. Thus, provision is made for the overwintering of immature insects in a state of developmental standstill. With the arrival of more favourable conditions, ecdysone is again secreted, and development resumes. Because many insect species have more than one generation of progeny per year, the prothoracic glands do not cease functioning except at some stage in the life cycle of the brood that must overwinter.

Dormancy in cold-blooded vertebrates

      Two kinds of dormancy can be distinguished in vertebrates on the basis of body temperature. Most vertebrates are poikilothermous, or cold-blooded, because the body temperature follows that of the environment and is not kept constant by internal (homoiostatic) mechanisms. The second group, the homoiotherms, maintain a constant body temperature regardless of the ambient temperature; these warm-blooded animals include birds and mammals.

Fishes and amphibians

      The metabolism of poikilothermous animals is most influenced by the environmental variables of temperature, nutrition, and photoperiod. Photoperiod, the daily length of light exposure, has a marked metabolic effect in both fishes and amphibians; fishes, however, remain active throughout the year, although the activity may be limited by temperature, as in those fish that rest on the bottom or in mud during cold periods. Brief superficial freezing and supercooling (without freezing) to temperatures below the freezing point of body fluids are experienced by resistant species, but it has not been established that fishes that have been frozen solid can become active when thawed. In the Arctic, no fishes are found in lakes that freeze solid in the winter. Because most fishes do maintain some kind of activity year round, they cannot be said to become dormant in the sense in which the word is used in this article.

      In addition to light and temperature, another environmental stress imposed upon fish is drought. Lungfishes (lungfish), as represented by the African lungfish (Protopterus), burrow deeply into the mud when their water supply is diminished. They surround themselves with a cocoon of slime and remain inactive. Their gills are nonfunctional during this period of dormancy, and they use a lunglike air bladder for respiratory purposes. They rely on fat reserves as an energy source, and in order to conserve water, they excrete urea rather than ammonia. This is because ammonia as an excretory (excretion) product is highly toxic; animals that excrete ammonia require large quantities of water to dilute it below toxic levels. Urea is a semi-solid substance of low solubility, and requires little or no water for its excretion. (Desert animals and many insects excrete urea.)

      During periods of drought or cold, amphibians (amphibian) seek protective niches in which to remain dormant until the return of favourable environmental conditions. Overwintering of frogs (frog) and salamanders frequently involves their aggregation in large numbers in a moist terrestrial niche, such as a rotting log, the mud on banks or bottoms of marshes and ponds, or in springs. The more terrestrially oriented amphibians, such as toads, may pass the winter in solitary burrows on land. During dry seasons, frogs may be dormant in a mud cocoon.

Reptiles (reptile)

Effects of temperature

      Because reptiles depend on external sources of heat to keep warm, they survive during periods of low temperature by seeking a place where the temperature will not fall below freezing, except temporarily. The commonest niche for reptilian dormancy is almost always found underground at a depth dependent on the thermal conductivity of the soil relative to the minimum temperature reached. This factor alone can control the distribution of reptiles. None can survive in the Arctic or Antarctic in places in which the subsoil is permanently frozen; and relatively few can exist in areas near these regions, even if suitable sites for dormancy were available, because the short summers would prevent the completion of life cycles. Although the distribution of snakes (snake) at high latitudes or altitudes is limited, the adder has been found at 3,300 metres (10,000 feet) in the Swiss Alps and as far north as the Arctic Circle. The Himalayan pit viper has been found at an altitude of 5,000 metres (16,000 feet).

      Dormancy in reptiles may display a circadian rhythm, a seasonal one, or both; it is a state of torpor directly induced by low temperature. When the adder, for example, experiences temperatures of about 8°–10° C (46°–50° F), it begins to search out suitable niches in which to rest. Its dormancy ends on the first sunny days after the maximum temperature has reached 7.5° C (45.5° F). Because these conditions vary, the adder's period of dormancy extends from 275 days in northern Europe to 105 days in southern Europe and is about two weeks in the United Kingdom, where the Gulf Stream provides warmth.

      Reptiles also normally become dormant during the hottest parts of summer, but the physiology of summer dormancy is quite different from that of winter. As already mentioned, winter dormancy is a state of torpor, induced by a low temperature, that becomes more pronounced as the temperature falls. There is, however, a wide range between the animal's normal, active (coenothermic) temperature and the lowest temperature at which it can exist. At high temperatures, on the other hand, there is a much narrower range between the coenothermic temperature and temperatures that cause death. In other words, reptiles can tolerate colder temperatures much better than they can tolerate higher ones. For this reason, during hot weather they must seek refuge underground or in cool, shady places, where they remain physiologically active but must forego all normal activity because of the restricted nature of the cooler niche. Desert reptiles, in particular, exhibit such temperature responses daily.

      During its dormancy, the amount of water needed by a reptile is less than at other times and is normally supplied by water produced from the metabolism of the animal's own stored food reserves, particularly fat. In areas in which alternating wet and dry seasons occur, reptiles maintain a longer period of dormancy during the dry season. This behaviour may be related more to the lack of available water than to temperature, because in such areas the onset of the seasonal monsoons elicits a period of increased reptile activity.

      Because there is only a limited number of suitable sites available for dormancy, several snakes, usually of the same species, may be found in each niche. As many as 100 or more snakes have been taken from one winter den. Occasionally, lizards and toads may also be found in the same den, but stories of snakes that share denning sites with small birds and mammals have been difficult to substantiate. It is much more usual to find that the entry of snakes into the burrow of a prairie dog or some other warm-blooded animal is followed by the evacuation of the original occupant.

Effects of latitude

      Changes in latitude not only alter the lengths of the dormant and active periods of reptiles but also affect their circadian rhythms because of the changes in the proportions of night to day. Many species of snakes, including the adder, are normally active in the early evening. In the northerly latitudes (e.g., northern Europe, such as Scandinavia and Finland), where the length of the active season is reduced by as much as two-thirds, these snakes are active throughout the day and are able to take advantage of every warm hour in order to complete the necessary portions of their life cycle. Even this increased activity during the shorter summer season, however, does not compensate for the latitude. Growth and development slow to such a point that sexual maturity is delayed, and the reproductive period requires two years rather than one; young are produced only every other year instead of every year, as at lower latitudes.

Dormancy, hibernation, and estivation in warm-blooded vertebrates

Homoiotherms and heterotherms

      The term hibernation is often loosely used to denote any state of torpor, inactivity, or dormancy that an organism might exhibit. Properly speaking, however, use of the term should be confined solely to warm-blooded (warm-bloodedness) homoiotherms; i.e., birds and mammals (mammal) whose feathers or fur serve as insulation to reduce heat radiating from the body and aid in the maintenance of constant body temperatures, which normally are independent of those of the environment. Because warm-bloodedness gives animals an internal physiological stability, they are less dependent on many environmental restrictions, particularly those limitations imposed on organisms by ambient temperatures. For example, only two species of reptiles are found north of the Arctic Circle, but great numbers of birds live and breed there. Warm-bloodedness also signifies a high metabolic rate, a factor that undoubtedly influences normal learning, which depends heavily on the frequency and recency of experiences. Because periods of lowered metabolism interrupt continuous learning experiences, they may explain in part why birds and mammals are so much easier to train than any other animal. The benefits of warm-bloodedness require the expenditure of large amounts of energy through the year and make a heavy demand on available food supplies.

      The term hibernation is also used to delineate the dormant state only during winter. In arid regions a reverse phenomenon is seen in which the animal becomes torpid during the hot, dry, barren summer; such hibernation is called estivation. As a means of avoiding environmental stresses, hibernation and estivation are not common devices among warm-blooded animals and they are far less common among birds than among mammals.

      Some warm-blooded organisms exhibit thermic instability, a heterothermous condition that allows their metabolic rate to be reduced, with a commensurate reduction in body temperature. Heterothermy is a transitional state between cold-bloodedness and warm-bloodedness; the animal is awake and moving during its temperature fluctuations. The body temperature, although not as constant as in humans, is not so low as to force the organism into deep hibernation. Among mammals, two monotremes, the spiny anteater and the duckbill platypus, are thermally unstable; many of the marsupials, including the opossum, the pouched mouse, and the native cat (a weasel-like spotted marsupial of the family Dasyuridae), are also unable to maintain a fixed body temperature.

      The true hibernator not only possesses adaptations that enable it to respond as a homoiothermous animal during certain periods of the year but can also adapt to stressful environmental situations and become essentially a poikilothermous animal during other periods. An animal exposed to food shortages, low temperatures, or lack of water, for example, may “turn off its thermostat” and hibernate until the environment becomes more favourable. Unlike poikilotherms, however, hibernators still retain a measure of temperature control and can change their metabolic levels as required. They can arouse themselves to full activity, whatever the environmental temperature, whereas the arousal of a poikilotherm is dependent upon increased environmental temperatures.

      During the period prior to hibernation an animal must make a considerable number of gradual physiological and metabolic adjustments that appear to be correlated with temperature, light, and the availability of food. No one set of conditions applies equally to all hibernators: some store food, others do not; some become excessively fat, others gain a more moderate amount of weight. Generally, as the season advances and as the hibernator becomes progressively more prepared for hibernation, there is an increase of fat deposition and a general readjustment of body temperature, metabolism, and heart rate to lowered levels of activity.

      Although no single factor or condition can be said to determine when an animal will go into hibernation, specific changes include an increase in the quantity of magnesium in the blood and a reduction in the activity of endocrine glands, such as the pituitary, thyroid, and adrenals. A reduction in gonadal activity has also been observed; hibernation does not occur when the gonads are in an actively functional state. Perpetuation of the species requires that the animal be warm and active during the mating and pregnancy periods.

      There appears to be a relationship between sleep and hibernation; available evidence suggests that hibernation is entered into from a state of sleep. If hibernation is to be considered a form of sleep, then it must be considered a remarkably complex one. Hibernation and sleep are somewhat similar in that essential body processes continue during both periods at a lowered level. In sleep, the heart beats less rapidly, and breathing is slower; the body produces less heat, necessitating that a sleeping person be protected from the cold.

Hibernation in birds (bird)

Temperature variations

      Birds normally have higher and more variable temperatures than do mammals. Whereas mammalian temperatures normally range between 36° and 39° C (97° and 102° F), avian temperatures range between 37.7° and 43.5° C (99.9° and 110.3° F), with the majority between 40° and 42° C (104° and 108° F). Although the nesting temperature of most passerine species (perching songbirds) is about 40.5° C (104.9° F), primitive bird species—like primitive mammals—have lower temperatures than do the more advanced species. The kiwi, for example, has an average coenothermic body temperature of 37.8° C (100° F). In general, the temperatures of small birds fluctuate more than do those of large birds. The temperature of a house wren (Troglodytes) may fluctuate 8° C (14° F) in 24 hours, that of a robin (Turdus) fluctuates about 6° C (11° F), and that of the domestic duck only about 1° C (2° F).

      The circadian period of activity and rest in birds is accompanied by a temperature cycle. Birds active in the daytime have their highest temperatures late in the afternoon and their lowest in the early morning. Nocturnal species, however, such as owls and the kiwi, have their maximum body temperatures at night, when they are most active. Seasonal temperature variations are also found in birds, and, like mammals, certain birds exhibit thermic instability. Although some are capable of maintaining a highly stable body temperature, others have a fluctuating body temperature. A torpid poorwill (Phalaenoptilus nuttallii) is an example of a bird that demonstrates both thermic instability and true hibernation. Its coenothermic body temperature is relatively constant; it can, however, through the influence of a thermoregulatory centre (the hypothalamus) in the floor of the brain, become essentially poikilothermous. Under such influence, its body temperatures approximate those of the environment.

Energy conservation

      Considering that hibernation and estivation are devices to avoid such factors as stressful extremes of temperature, lack of water, unavailability of food, or lessened photoperiod, they also must be energy-conservation devices for the animals concerned. Even short periods of torpor can conserve energy. The efficiency of this energy-conservation system can be demonstrated by comparing the smallest bird, the hummingbird, which exhibits circadian torpor, with the shrew, the smallest mammal, which remains active throughout a 24-hour period. Oxygen consumption is an indicator of metabolic rate, and at an environmental temperature of 24° C (75° F) during the day, an awake but resting hummingbird consumes about 14 millilitres of oxygen per gram per hour. At dusk, the rate drops first to a sleeping level and then plunges to a torpid level of about 0.8 millilitre of oxygen per gram per hour. Just before daybreak, the bird awakens for another activity period. The hummingbird has the highest metabolic rate and the greatest metabolic range of any vertebrate. The shrew, in contrast, consumes about the same amount of oxygen as the hummingbird does during the day and even increases the amount slightly at night.

      The hummingbird uses about 10.3 calories (units of heat energy) during each 24-hour period if it sleeps at night without becoming torpid but only 7.6 calories if it becomes torpid. As it wakes from the torpid state, its temperature increases about 1° C (2° F) per minute to a maximum; the entire process takes less than 30 minutes and sometimes as little as 10 minutes. The energy required to warm the tissues of the hummingbird is relatively small; a hummingbird that weighs four grams expends only 0.114 calorie to warm its body from 10° to 40° C (50° to 104° F). This is only ¹/₈₅ of the total 24-hour expenditure of energy of a hummingbird in nature.

      The behaviour of the hummingbird can be contrasted to that of a larger bird, such as the poorwill, which is a nocturnal, insect-catching bird. During an average 24-hour day, the poorwill has brief periods of activity at dusk and just before dawn, the total of which is scarcely more than an hour. The temperature of the poorwill during these periods of activity, which are correlated with the bird'sfeeding habits, is between 40.5° and 43.1° C (104.9° and 109.6° F). Between periods of activity, the bird rests quietly, and its body temperature drops 1° to 3° C (2° to 5° F).

      During periods when a supply of flying insects is not available, the bird hibernates in depressions in rocks or other suitably protected places, to which it returns each year. When hibernating, the bird's temperature is frequently within 1° C (2° F) of that of the environment; as a result, the energy saved is great. A poorwill whose body temperature is 5° C (41° F) has a metabolic rate only 3 percent of its metabolic rate at normal body temperature. Because the poorwill is a larger bird than a hummingbird, it may take more than an hour for it to emerge from hibernation.

Types of hibernation in mammals

      It takes longer for larger animals than for smaller ones to go into hibernation because heat must radiate from the body before the temperature can be lowered. Thus, it would require a considerable amount of time for large birds or mammals to go into and emerge from hibernation each day, as do bats and hummingbirds. A 200-kilogram (440-pound) bear, for example, would need 5,100 calories to warm from 10° to 37° C (50° to 99° F). Unlike the hummingbird, which uses only ¹/₈₅ of its total daily energy expenditure to emerge from hibernation, the amount expended by a bear would be equivalent to its full 24-hour energy budget. Even if there were enough time in 24 hours for a large animal to enter into and emerge from dormancy, therefore, it would be metabolically extravagant, thus defeating a purpose of hibernation.

      Actually, the most common misapplication of the term hibernation is in relation to the bear, which is not a true hibernator. Its body temperature, which normally averages 38° C (100° F), drops during its winter lethargy to about 34° C (93° F), seldom getting below 31.2° C (88.2° F). Hence, a bear's temperature during the winter does not approximate that of the environment. This is indicative of winter rest rather than true hibernation. During this inactive period, the bear sleeps but is, nonetheless, warm and capable of activity when stimulated, unlike a true hibernator. Moreover, it is also during this period when females give birth to cubs that suckle and are maintained by maternal warmth until they emerge from the den in the spring. This behaviour is in contrast with that of the Arctic ground squirrel, whose normal temperature is the same as that of the bear but whose temperature during hibernation drops to near freezing and, in some cases, to a degree or two below 0° C (32° F).

      Although certain mammals are said to hibernate, they do not necessarily enter a state of deep hibernation during winter. Instead, for weeks at a time they may be inactive and lethargic in behaviour, with a slightly depressed body temperature. The chipmunk (Eutamias) is an example of what has been termed a shallow hibernator, as are bears and raccoons. Superficial hibernation, apparently a compromise between the minimum energy requirements of a deep hibernator and the high energy expended by an animal that remains active during the winter, saves energy without the stress of hibernation. The animal can thus conserve food, while still being able to escape from predators and such dangers as flooding of its burrow. The main energy source during the winter in this shallow hibernation state is food stored in the winter nest. There are instances, however, of shallow hibernators, such as the chipmunk, that enter a state of deep hibernation, particularly if without food.

True mammalian hibernation

      Omitting the thermally unstable mammals, the true mammalian hibernators are those whose lowered body temperatures approximate that of the environment and those who require extensive and complex physiological changes to turn from a warm-blooded animal into an essentially cold-blooded one for an appreciable length of time. Only three orders of placental mammals display such behaviour: the Insectivora, as exemplified by the hedgehog; the Chiroptera, the bats; and the Rodentia, including the marmot, hamster, dormouse, hazel mouse, and ground squirrel.

      A typical mammalian hibernator, such as the Arctic ground squirrel, finds a protected environmental niche—in this case, a burrow beneath the surface—and builds a nest of grass, hair, and other materials to provide still further insulation. The usual hibernating position is one of being curled up in a ball with the extremities tucked tightly against the body so there is a minimal surface-to-volume ratio. After the temperature of the animal has dropped near that of the ambient temperature, it appears to be dead: its respiration is imperceptible, about three irregular breaths per minute; it does not react to outside stimuli in an observable fashion; nor does it react to being handled and uncurled, although such handling will trigger wakening mechanisms.

      The internal organs, such as the digestive tract and the endocrine glands, are almost totally inactive. Because the process of hibernation necessitates the mobilization of all body resources, it places great demands on the tissues, all of which are directed toward the problem of maintaining the animal's metabolism at the minimal level necessary for life during the hibernating period. This means that all activity not immediately germane to the process of living at the lowest possible metabolic level ceases. Even bones and teeth deteriorate during hibernation. The hibernator apparently is balanced on a very narrow line between the maintenance of life at a level that makes recovery from hibernation possible and a reduction of metabolism to a level that will lead to death. Evidence obtained from tissues indicates that the process of hibernation is a precarious method of survival at best and one from which many animals do not awaken. As a mechanism of species survival, hibernation seems effective; for the survival of the individual, however, it is an uncertain and dangerous process.

      The hibernator does not remain in a continuous state of hibernation from the time it enters in the fall until it emerges in the spring. Hibernating Arctic ground squirrels, for example, awaken at intervals of every three weeks or less. During this time the animals may move about and sometimes emerge from the burrow. These periods of arousal are more frequent at the beginning and end of a hibernation period than in mid-hibernation; and the lower the temperature at which an animal hibernates, the fewer the awakenings.

      During the period of hibernation about 40 percent of the total body weight is lost, an average of about 0.2–0.3 percent per day. One period of arousal and wakefulness consumes more heat and energy than many days in hibernation. About 90 percent of the total heat production and weight loss during hibernation takes place during the arousal periods; only 10 percent is required to maintain the animal in hibernation. Thus, in the case of an unusually long or hard winter, the animal may be called upon to use all of its available energy sources in periodic arousals; it then enters one final hibernation period from which it does not awaken. Animals that store food in the nest have a chance to renew their energy requirements by eating when they awaken periodically.

Entrance into hibernation

      Hibernating mammals can be divided into four major groups according to the way they enter hibernation. One group is exemplified by the golden hamster; it waits a variable time of from one to three months in the cold and then enters hibernation in one major temperature reduction. This is accomplished when the biochemical and physiological preparations have been sufficient to lower the animal to a level at which it is receptive to the hibernating stimulus, which causes the abandonment of the temperature differential between ambient and body temperatures.

      A second group, of which the pocket mouse (Perognathus) is an example, prepares for hibernation relatively rapidly, waiting only a few days before becoming torpid in one major temperature decline. The third group, which constitutes most of the mammalian hibernators, includes ground squirrels (ground squirrel) and marmots (marmot). These animals wait only a few days before entering hibernation and then go through a series of steps of torpor and arousal, each one at successively lower body temperatures, until the level dictated by the stage of preparation for hibernation is reached.

      The fourth group, which includes most of the bats (bat), becomes inactive in the poikilothermous manner; that is, the body temperature follows the ambient temperature. Even though the bat seems ready to hibernate at any season, survival during hibernation depends upon more adequate preparation than is necessary for the transitory periods of torpor. Bats not only exhibit true hibernation during the winter but also have natural periods of hypothermia (subnormal temperature), which are unrelated to hibernation, during the remainder of the year.

      The woodchuck (woodcock), the dormouse, and the California ground squirrel enter hibernation in successive stages, with a complete or nearly complete awakening between each one. In the woodchuck, an initial decline in temperature is followed by an arousal. During the second decline there is a lower and more pronounced fall in body temperature, followed by a less pronounced rise. This process continues until the body temperature is essentially the same as that of the environment.

Physiological changes during mammalian hibernation

heart rate and circulation

      The body temperature of a hibernating mammal is affected by changes in respiration, heart rate, and oxygen consumption; all are apparently mediated by a part of the nervous system. The heart rate decreases prior to a decline in body temperature. In the woodchuck, the rate may drop from 153 to 68 heartbeats per minute within 30 minutes. In the California ground squirrel, the heart may beat as slowly as once a minute at 5° C (41° F). In contrast, the hearts of non-hibernators generally will not beat at all at temperatures below 10°–20° C (50°–70° F).

      As an Arctic ground squirrel prepares for hibernation, its heart rate and its blood pressure decrease. Both may be detected before a decrease in body temperature can be noted. When the animal enters hibernation, temperatures of both the heart and abdominal regions are identical, indicating an even blood flow between the anterior (front) and posterior (rear) parts of the body. As the body temperature drops, the resistance to blood flow in the peripheral parts of the circulatory system increases because of the increased viscosity (resistance to flow) of the chilled blood and the constriction of the distal arterioles (small arteries) of the body. This peripheral resistance maintains blood pressure at relatively high levels in the deeply hibernating squirrel, even when the heart beats only three or four times a minute.

Neural changes

      The nervous system of hibernators also is acclimated; certain specific structures and pathways are seemingly maintained to regulate and coordinate metabolism as temperatures drop. This adaptation of the nervous system enables changes in the environment to be perceived, even when the animal is torpid. In the Arctic ground squirrel, measurements of the general electrical activity of the brain indicate a 90 percent reduction when the animal is in hibernation, at which time brain temperatures approximate 6° C (43° F). During hibernation, both the peripheral nervous system (all the nerves outside the brain and spinal cord, which constitute the central nervous system) and the spinal cord have an increased sensitivity to certain stimuli; in addition, the areas of the brain that regulate temperature as well as cardiac (heart) and respiratory function remain active at ambient temperatures, below which the mammalian nervous system normally ceases to function.

      Changes in the circulatory system involving constriction (narrowing) of posterior vessels and the favouring of anterior circulation allow the brain temperature of hibernators to remain a few degrees warmer than the environmental level. This enables the temperature of the brain to remain constant despite fluctuations in the temperature of the skin.

Endocrine activity

      The male sex hormone testosterone stimulates reproductive activity. The golden hamster will not hibernate if injected with more than five milligrams of a hormonal preparation. Hibernation is also prevented if the animal is fed or injected with thyroid (thyroid gland) hormones or thyroid-stimulating extracts. The latter would seem to implicate the thyroid as another endocrine gland that plays an important role in hibernation. There is, in fact, a seasonal progression and regression of thyroid activity in hibernators; maximal activity occurs in the spring and minimal activity in the fall. And because hibernation does not take place in the absence of the adrenal glands, it appears that a minimal adrenal activity is also necessary for hiberation and survival.

      The importance of timing in the annual rhythm of activity and dormancy can be demonstrated: when hibernators are exposed to cold temperatures in spring and summer, they react as do all homoiotherms by increasing their thyroid activity and metabolic rate to maintain normal body temperature. But if they are exposed to cold temperatures in the fall, the thyroid activity and metabolic rate of hibernators are lowered. In some species, a combination of decreased food and lower ambient temperature is required to reduce activity of the thyroid gland and to produce hibernation, although cold alone is sufficient in ground squirrels and the dormouse.

      Although hibernation does not take place during periods of gonadal activity or stimulated thyroid activity, it can occur during increased activity of the pituitary gland. This would suggest that there is a dissociation of cellular growth and hormone synthesis that is normally controlled by hormone secretion of the pituitary and its target organs. Thus, the triggering mechanism for the resumption of normal endocrine activity apparently resides elsewhere than in the pituitary. The function of the hypothalamic (hypothalamus) region of the brain in regulating appetite, fat deposition, water intake, and diuresis (increased excretion of urine), as well as in the control of temperature and sleep, would appear to make it a key area in directing life processes of the hibernator. Furthermore, the fact that the hypothalamus regulates the pituitary and other endocrine glands not only supports this thesis but also indicates that this area of the brain is the prime, or master, regulator of the entire hibernation process.

Reproductive (reproductive behaviour) cycles

      The Arctic ground squirrel may spend more than half its life in hibernation. It thus must be able to breed, rear young, maintain its home burrow, and prepare for the period of hibernation during an activity period of less than six months. This requires considerable adaptation of both metabolic and behavioral patterns. Prior to entering hibernation in late September or early October, there is a renewal of sexual activity in the testes of males, and, throughout the period of hibernation, they continue to grow. On the Arctic slope in early May, the male ground squirrel emerges from its burrow. As it utilizes the remaining fat and eats the stores of seeds and other food still in the nest, the male reaches a period of reproductive readiness. Mating takes place in the middle of May, and the young are born in the middle of June, after a gestation period of about 25 days. By the middle of July the young are above ground and eating the green Arctic vegetation, which they continue to eat until the onset of hibernation. By October, both the young of the year and the adults from the previous year weigh nearly 1,000 grams (2.2 pounds).

      In the bat, the reproductive cycle is interrupted by hibernation. Gonadal activity in the male reaches its maximum in the fall, when copulation with the female occurs. The animals then hibernate, and the production of sperm in the male ceases. The sperm deposited in the female are stored in her reproductive tract throughout the period of hibernation; fertilization occurs the next spring, when the eggs are ovulated (released from the ovaries) within a few days after awakening from hibernation.

      The only exception to the general hibernation–reproduction pattern of bats is the vespertilionid bat (Miniopterus), in which there is no delayed ovulation and fertilization. In this species the eggs are ovulated soon after copulation, in the fall, and fertilized immediately. During the ensuing period of hibernation embryonic development is initiated and slowed, but it does not actually cease. The young are born in the early summer, soon after hibernation ends. The introduction of hibernation during pregnancy makes the gestation period several months longer than in non-hibernating tropical members of the same genus.

      Cyclical reproductive activity has thus become adapted to the shortened activity season available to the hibernator. But although the annual sequence of reproductive events is known, the external stimuli that regulate the reproductive cycles of bats and other hibernators are not known. More knowledge is needed concerning the endocrine and nervous mechanisms that presumably regulate reproductive processes internally. It has been suggested that the pituitary–gonadal relationship influences the hibernating cycles as well as the reproductive cycle, hence both the latter and homoiothermism are controlled by a common mechanism. Such a suggestion is attractive in that the mechanism solves the regulation problems, but more needs to be known of the way in which hibernation directly or indirectly modifies the action of endocrine and neural mechanisms that direct the reproductive cycle.

Protection from disease and radiation

      Hibernating organisms have a certain degree of resistance to infectious diseases (animal disease) that appears to be attributable to at least three factors, all of which are related to temperature. One is the fact that the lowered temperature of the host and the commensurate slowing of its metabolic processes prevent the multiplication of parasites to a greater extent than they affect the host's defensive mechanisms. Second, lower temperatures are more harmful to the development of a disease organism than to the host, as has been shown with the parasite Trichinella spiralis. In bats hibernating at 5° C (41° F), only larvae have been recovered from the intestines; but mature adult worms have been recovered from the intestines of bats kept at 35° C (95° F). The third factor is that the influence of low temperature on the chemical composition of the host tissues may also affect infectious organisms.

      Hibernation also seems to protect animals from radiation. When ground squirrels are irradiated with radioactive cobalt while hibernating, they are found to be more resistant to the effects of the radiation than are squirrels irradiated while warm and active. This resistance, which is apparent over a wide range of doses, suggests that protective mechanisms function in the hibernating animal. In both hibernating and non-hibernating animals, repair processes within cells occur the first day after irradiation; however, when the metabolic requirements of cells are small, as in hibernation, the injured cells seem to be more capable of repair, and survival is greater. The large metabolic (metabolism) requirements imposed on injured cells of warm and active animals appear to render them incapable of an adequate repair response.

Awakening from hibernation

      The process of awakening in the Arctic ground squirrel takes about three hours. There is a rapid rise in heartbeat and a decrease in peripheral circulatory resistance; the area around the head and heart warms more rapidly than the posterior part of the animal. This differential vasodilatation (widening of the blood vessels) in the anterior part of the body is a unique and vital part of the awakening process. The concentration of active circulation in this region results in a high blood pressure and an efficient and rapid warming. If a drug is administered during awakening that causes vasodilatation throughout the body, there is a marked drop in blood pressure even though the heart may almost double its rate; thus, the heart cannot maintain a high blood pressure at this time if all blood vessels are dilated. Later during the arousal process, after the anterior part of the body has been warmed, the posterior part of the animal warms rapidly.

      Despite the deterioration of glands and tissues and the drastic reduction of all metabolic activity during hibernation, within 24 hours after arousal, all the squirrel's physiological processes are essentially normal. This rapid repair and recovery mechanism is one that requires further study.

William Vernon Mayer Ed.

Additional Reading

Dormancy and related mechanisms are treated in Charles P. Lyman and Albert R. Dawe (eds.), Mammalian Hibernation (1960), examining hibernation and hypothermia in birds and mammals, including articles on such thermally unstable forms as bears; Charles Kayser, The Physiology of Natural Hibernation (1961), an intensive look at hibernation in birds and mammals, including hypothermia and estivation, with emphasis on functional changes; John P. Hannon and Eleanor Viereck, Comparative Physiology of Temperature Regulation (1962), dealing with temperature regulation in both cold- and warm-blooded animals, including hypothermia and hibernation; William V. Mayer, Hibernation (1964), a brief, popular treatment of both birds and mammals; Kenneth C. Fisher (ed.), Mammalian Hibernation (1967), symposium papers dealing directly or indirectly with the topic of mammalian hibernation accompanied by over 1,300 bibliographical references relative to this topic; X.J. Musacchia and Joseph F. Saunders (eds.), Depressed Metabolism (1969), a variety of studies relative to hibernation, hypothermia, and thermic instability; and Harold W. Woolhouse (ed.), Dormancy and Survival (1969), a symposium incorporating a wide variety of review articles covering dormancy in a broad spectrum of organisms, from bacteria through mammals.

* * *