Respiration appears to be totally suspended in animals in a complete state of hibernation, if left undisturbed. It may however, be readily re-excited by the slightest stimulus; and to this fact may perhaps be attributed the belief that breathing does not actually cease. If a hibernating hedgehog be lightly touched it draws a deep breath, and breathing is maintained for a longer or shorter time before again ceasing; but if at the same time the temperature of the atmosphere be raised, respiration becomes continuous and lethargy is succeeded by activity (Marshall Hall). The opinion that respiration is totally suspended is supported by a number of facts. Hibernating marmots and bats, for example, have been known to live four hours in carbon dioxide, a gas which proves almost instantly fatal to mammals in a state of normal activity (Spallanzani). A hedgehog which may be drowned in about three minutes when awake and active, has been removed from water uninjured when in deep winter sleep after twenty-two and a half minutes’ submergence. A hibernating noctule bat, when similarly treated, survived sixteen minutes’ immersion. Further proof of the suspension of respiration has been furnished by experiments upon a bat which while in a deep and undisturbed state of lethargy was kept in a pneumatometer for ten hours without appreciably affecting the percentage of oxygen in the air. The same animal, when active, removed over 5 cub. in. of oxygen in the space of one hour from the instrument.
As in the case of respiration, alimentation and excretion are suspended during hibernation.
The circulation of the blood, on the other hand, continues without interruption, though its rapidity is greatly retarded. This fact may be observed by microscopic examination of the wings of bats in a state of winter sleep. Moreover, in the case of a hedgehog lethargic from hibernation, it was experimentally shown that when the spinal cord was severed behind the occipital foramen, the brain removed and the entire spinal cord gently destroyed, the heart continued to beat strongly and regularly for several hours, the contraction of the auricles and ventricles being quite perceptible, though feeble, even after the lapse of ten hours. After eleven hours the organ was motionless; but resumed its activity when stimulated by a knife-point. Even after twelve hours both auricles responded to the same stimulus, though the ventricles remained motionless. Shortly afterwards the auricles gave no response. On the other hand, when the spinal cord of a hedgehog in a normal state of activity was severed at the occiput, the left ventricle ceased to beat almost at once, and the left auricle in less than fifteen minutes; the right auricle was the next to cease, whereas the right ventricle continued its contraction for about two hours. Experiments upon marmots have yielded very similar results. The heart of a marmot decapitated in a state of lethargy continued to beat for over three hours. The pulsations, at first strong and frequent and varying from 16 to 18 per minute, became gradually weaker and less frequent, until at the end of the third hour only 3 were recorded in the same length of time. Excised pieces of voluntary muscular tissue contracted vigorously three hours after death under electric stimulus. Only at the end of four hours did they cease to respond. The heart of an active marmot killed in the same way contracted about 28 times a minute at first, the number of pulsations falling to about 12 at the end of fifteen minutes, to 8 at the end of thirty minutes, and ceasing altogether at the end of fifty minutes. Similarly the response of the muscles to galvanic shock failed at a correspondingly rapid rate. It is evident, therefore, that during hibernation the irritability of the heart is augmented in a marked degree, and that the irritability of the left side of the organ is scarcely less pronounced than that of the right side. Similar reduction in the rate of the circulation has been demonstrated in certain hibernating mollusca, Mr C. Ashford having proved experimentally that the number of pulsations of the heart per minute gradually lessens with a falling temperature. At a temperature of 52° F. the number was 22 in the common garden snail (Helix hortensis), and 21 in the cellar slug (Hyalinia cellaria). At a temperature of 30° F. the pulsation fell to 4 in the former and to 3 in the latter animal.
The nature of hibernation, and probably also of aestivation, and the principal physiological phenomena connected with them, may be briefly summarized as follows:—
1. During hibernation death from starvation and wasting of the tissues is prevented by the absorption of fat, which, at least in the case of mammalia, is stored in considerable quantities, sometimes in definite parts of the body, during the weeks of activity immediately preceding the period of winter sleep.
2. Every gradation seems to exist between ordinary sleep and hibernation; the differences between the ordinary diurnal or nocturnal sleep in summer of hibernating animals and their prolonged and lethargic quiescence in winter are merely differences of degree, differences, that is to say, of intensity and duration.
3. The physiological accompaniments of hibernation are: (a) Cessation of all activities associated with alimentation and excretion; (b) lowering of the body temperature to that of the surrounding medium or to within a few degrees of it; (c) total or almost total cessation of respiration, accompanied by power to survive immersion for a considerable time in water or asphyxiating gases, which prove rapidly fatal to the same animals when normally active; (d) marked increase in the irritability of the muscles, especially of those of the left side of the heart, whereby the pulsations of that organ, although retarded, are uninterruptedly maintained; (e) a slight exchange of gases in the lungs is kept up by the cardio-pneumatic movement.
4. Amongst cold-blooded animals, both vertebrate and invertebrate, devoid of the faculty of temperature adjustment, the phenomenon of hibernation or aestivation is of general occurrence wherever the conditions of existence accompanying the onset of cold or drought are inimical to active life. In hot-blooded vertebrates, on the contrary, the phenomena are non-existent so far as birds are concerned; aestivation is of very rare occurrence in mammalia, while hibernation is practised by a comparatively small number of species; and in these the faculty of temperature adjustment appears to be temporarily at all events in abeyance.
II. The Zoology of Hibernation and Aestivation.—Owing to the extreme difficulty of keeping wild animals under observation in their natural haunts for any lengthened time, it is almost impossible to get accurate knowledge of the details of this state of existence. In a general way it is known, or assumed from their disappearance, that certain species retire to winter quarters in particular districts, but on such important points as whether the winter sleep is continuous or interrupted, light or profound, assured information is for the most part not forthcoming. This is true even of familiar species inhabiting Europe and North America, which have been objects of study for many years. It is still more true of species occurring in countries uninhabited and rarely visited, especially in winter, by naturalists interested in such questions. The Chiroptera (bats) furnish an illustration of this truth. It was formerly assumed that the winter sleep of these animals in north and temperate Europe was complete and uninterrupted. Marshall Hall, for example, remarked that “perhaps the bat may be the only animal which sleeps profoundly the winter through without awaking to take food.” It was known, it is true, that in countries where gnats and other winged insects disappear with the first frosts of winter, bats which feed upon them retire to winter quarters in hollow trees, caves, sheds or other places likely to afford them sufficient shelter. Here they hang suspended, solitary or in companies according to the species. But a mild spell of weather in mid-winter will sometimes entice a few to take wing while it lasts, although they never appear in any numbers until crepuscular and nocturnal insects are plentiful. But Mr T. A. Coward has recently shown in the case of the greater and lesser horseshoe bats (Rhinolophus ferrum-equinum and R. hipposiderus), that during the early period of their occupation of the winter retreat, hibernation, in the strict sense of the word, does not take place, and that even later in the season the sleep is constantly interrupted, especially when the temperature of the air rises above 46° F., and that during their wakeful intervals they crawl about and feed apparently upon the insects which live throughout the year in the caves. This is also true of the long-eared bat (Plecotus auritus), and probably of other species of this group. At Mussoorie in the Himalayas, and in other parts of northern India, insectivorous bats, such as Rhinolophus luctus and Rh. affinis, pass the winter in a semi-torpid state, and are rarely seen abroad during the cold season. The fruit-eating bats, on the contrary (Pteropidae), which are more southern in their distribution and are restricted in the Himalayas to the warmer valleys and lower slopes of the mountains, are as active in the winter as at other times of the year (Blanford).
Although almost as exclusively insectivorous as bats, moles and shrews do not, so far as is known, hibernate. This distinction between two groups so nearly alike in diet, no doubt depends upon the difference in their habitats and in those of the creatures they live upon. By tunnelling deeper in winter than in summer, moles are still able to find worms and various insects buried in the earth beyond the reach of frost; and shrews hunt out spiders, centipedes and insects which in their larval, pupal or sexual stages have taken shelter and lie dormant in holes and crannies of the soil, beneath the leaves of ground plants or under stones and logs of wood. In view of the perennially active life of the two insectivora just mentioned, it is a singular fact that the common hedgehog (Erinaceus europaeus)—the only member of this order besides genera referable to the moles (Talpidae) and shrews (Soricidae) that inhabits temperate and north-temperate latitudes in Europe and Asia—passes the winter in a state of torpor unsurpassed in profundity by that of any species of mammal so far as is known. Possibly the explanation of this seeming anomaly may be found in the bionomial differences between the three animals. The subterranean feeding habits of the mole render hibernation unnecessary on his part. Therefore the shrew and the hedgehog, both surface feeders for the most part, need only be considered in this connexion. As compared with shrews, amongst the smallest of palaearctic mammals, the hedgehog is of considerable size. Moreover, in point of vivacious energy it would be difficult to find two mammals of the same order more utterly unlike. Hence in winter when insects are scarce and demand active and diligent search, it is quite intelligible that the shrews, in virtue of their smallness and rapidity of movement, are able to procure sufficient food for their needs; whereas the hedgehogs, requiring a far larger quantity and handicapped by lack of activity, would probably starve under the same conditions. Like the common hedgehog of Europe, the long-eared hedgehog (Erinaceus megalotis) hibernates in Afghanistan from November till February. The tenrec (Centetes ecaudatus), a large insectivore from Madagascar, aestivates during the hottest weeks of the year; and specimens exhibited in the Zoological Gardens in London preserved the habit although kept at a uniform temperature and regularly supplied with food.