Hibernation:
Among the mammals, hedgehogs, dormice (Nuscardinus avellanarius and Glis glis) and bats (Chiroptera) represent the only true British hibernators. Contrary to popular misconception, hibernation is not simply a long period of sleep, although certain features of hibernation (e.g. body temperature and breathing regulation) do resemble those observed during slow-wave sleep. Sleep is a physiological necessity; it’s time during which our body exhibits increased cellular anabolism and decreased catabolism – in other words, sleep allows our body to repair and replace cells. There is no universally-presiding theory as to the function of sleep, but aside from providing much needed ‘downtime’ for the body to repair itself, it also seems to be required for anatomical development, consolidation of memory (spatial, procedural and declarative) and may even help to keep the animal safe (sleep at night when most predators are hunting). In humans, sleep deprivation leads to various physical and mental problems; infants deprived of sleep are known to exhibit decreases in brain mass and increased neuronal necrosis (nerve cell death). According to the Australasian Sleep Association in Sydney, the current official record for the longest period spent awake is 18 days, 21 hours and 40 minutes, with the ‘winner’ reporting hallucinations, blurred vision, slurred speech as well as lapses in memory and concentration – lethargy, irritability and even anorexia are known in long-term insomniacs.
While sleep appears to be physiologically essential (the case of Vietnamese livestock farmer Thai Ngoc, who apparently hasn’t slept since a bout of fever more than 30 years ago, being rather exceptional), hibernation is an adaptation to climatic conditions – it is by no means essential and is actually an inherently dangerous undertaking, although the likelihood of survival seems to increase significantly for subsequent hibernation episodes.
Hibernation is a major physiological readjustment with the goal being to reduce the animal’s metabolism (in the case of mammals, by turning down their internal ‘thermostat’), thereby conserving precious energy stores during periods when food is in short supply – it is energetically expensive to maintain a body temperature higher than the ambient (especially for poorly-insulated animals like hedgehogs) and decreasing the body temperature slows down the rate of biochemical reactions. Indeed, in his New Hedgehog Book, Pat Morris notes that hibernation occurs in response to any dramatic and prolonged food shortage, not necessarily only during the winter. Moreover, Desert hedgehogs (Paraechinus) will undergo hibernation if translocated to a cooler climate.
The plasticity of hibernation is well illustrated by hedgehogs. At the northern extent to their range, hogs may hibernate for more than 200 days, while in warmer climates (for example, in parts of New Zealand) they may forego hibernation altogether. Consequently, there are no fixed dates between which hedgehogs hibernate – this winter (2006 / 2007), Linda Fuller tells me that at least one of her resident hogs, DJ, didn’t hibernate, opting instead to eat her way through a whole can of dog food per night! Unfortunately, the bulk of hedgehog hibernation studies have been conducted in captivity and we still have relatively few data from wild specimens.
Following the breeding season, hedgehogs spend the bulk of their time feeding voraciously, laying down the fat reserves that will sustain them during hibernation. In a single evening, a hog may consume 20% of its body weight, drinking more than 300 ml in a single sitting. The result is that immediately prior to entering hibernation, a hedgehog is likely to weigh at least 600 grams and 30% of the hog’s bodyweight may be fat. The fatty tissue observed in hedgehogs at this time of year is of two distinct types: Brown Adipose Tissue (BAT or Brown Fat, which despite its name is actually more orange in colour owing to a mixture of different cytochromes) and White Adipose Tissue (WAT or White Fat). These tissues differ both in their biochemistry and structure as well as in their location in the body. BAT is stored around the shoulders, chest, neck and under the front legs; it may represent 3% of the hedgehog’s bodyweight immediately prior to hibernation. WAT is found subcutaneously (under the skin) and along the gastrointestinal tract (around the stomach and intestines).
Males enter hibernation earlier than females, because they have had more time after mating to build up their fat reserves, although (as mentioned) there are no set dates for the initiation of hibernation. Indeed, the factors involved in inducement of hibernation have long been eagerly sought and contested by biologists. Data from studies on captive hedgehogs suggest that hibernation is predominantly governed by persistent cold temperatures and Herter Konrad found that his captive hogs entered hibernation when the ambient temperature was between 15oC and 17oC (59 – 63oF) – it should be noted that these temperatures do not appear to be universal and one study published in 1964 reports that hogs from Finland tolerated lower pre-hibernation temperatures than their German conspecifics. In The Hedgehog, Pat Morris states that hedgehogs must be kept at between 15oC and 20oC (59 – 68oF) in order to remain active. Still, although temperature seems to be a highly significant influence for hedgehogs, several studies have presented data suggesting a molecular control of hibernation. Studies on hibernating Ground squirrels (Spermophilus lateralis) by Standford University’s Thomas Kilduff have suggested that there may be a protein regulating torpor in this species, implying the presence of a potential hibernation-inducing factor. However, not all data agree and, as Aline McKenzie put it in her review article to BioScience in 1990: “A hibernation-inducing factor is one of the holy grails of the field, with conflicting reports as to its sighting.”
Regardless of its cause, hibernation itself is typified by several physiological changes: a decrease in heart rate; lowering of peripheral body temperature; reduced breathing rate punctuated by apnoea (brief cessation in breathing); reduced metabolism sustained by fat reserves; and changes to the normal rate of function in key homeostatic organs.
An active European hedgehog will have a body temperature between 33oC and 37oC (91 – 99oF) -- varying with their circadian (24 hour) rhythm --, averaging 35oC (95oF) and falling to ~10oC (50oF) during hibernation. In a paper to the Journal of Comparative Physiology during 1990, Paul Fowler and Paul Racey (both at Aberdeen University) provide a fascinating insight into the changes of hedgehog body temperature over a daily and seasonal timescale. The zoologists inserted temperature sensitive radio transmitters into the abdomen of their subjects and found that changes in body temperature (TB) over a circadian timescale were closely tied with the photoperiod (maximum TB occurred two hours after midnight). Also, TB was closely matched with the ambient temperature during hibernation but TB showed a marked increase when the surrounding air temperature fell below -5oC (23oF), although arousal did not always follow (see below). The data show that the ‘average hedgehog’ entered hibernation at just before 2am and came out of hibernation at just before midnight. More interestingly, the results of these experiments show that the hedgehogs underwent spontaneous bouts of what the authors term “transient shallow torpor” (or TST). The observation that the bulk (80%) of TST events were recorded in August (although events were recorded throughout the year) suggests that they may serve as some kind of ‘physiological preparation’ for the main event, although TST bouts immediately preceded hibernation in only 20% of cases.
The heart rate of active hogs varies in accordance with prevailing conditions; still, electrocardiographic studies have demonstrated that most active hedgehogs have a heart rate of between 190 and 280 bpm (beats per minute), dropping to ~147 bpm in sleeping animals and averaging just under 14 bpm during hibernation. In conjunction with changes to the heart rate, hedgehogs entering hibernation seem to exhibit hypovolaemia (decrease in blood volume). In his 1961 paper to Nature, Einar Eliassen quotes a reduction in blood volumes of 8% body weight and 2% to 3% bodyweight for active ‘summer’ animals and “sleeping” winter animals, respectively. However, Dr. Eliassen notes that these figures may not be entirely accurate and he may actually have witnessed “pronounced differences in blood-flow in different vascular areas”. Nonetheless, there does seem to be a decrease in the animal’s blood volume and it appears to be linked with haemolysis (destruction of blood cells) and plasma excretion.
Foraging hedgehogs breathe at about 50 brpm (breaths per minute); this rate halves when resting and averages 13 or less during hibernation (at 4oC / 32oF). Hibernation is also punctuated by periods when breathing cessates completely (i.e. apnoetic events); these periods are typically brief, lasting only a few minutes -- although one study published in 1964 reported apnoetic events lasting two-and-a-half hours in Erinaceus europaeus -- and are punctuated by periods of rapid ventilation lasting between three and 30 minutes. Apnoeic events serve to reduce water loss (evaporation across the lungs) and conserve energy; cessation of breathing leads to a progressive acidification of the blood (a result of the build-up of carbon dioxide), which inhibits glycolysis (the breakdown of glucose).
During hibernation, the hedgehog is sustained by the (very slow) metabolism of its WAT fat reserves (i.e. through lipolysis). Torporic individuals may exhibit a metabolism only one or two percent of their active state and the virtual cessation of carbohydrate metabolism means that there are very low levels of blood insulin and glucagons (pancreatic hormones that control glucose metabolism), which manage the metabolism of glycogen (a chain of glucose molecules often referred to as ‘animal starch’). Indeed, carbohydrate metabolism begins shutting down before hibernation is fully underway; in his book Hedgehogs, Nigel Reeve notes that a hedgehog at the onset of hibernation may have undergone a 43% reduction in blood sugar level compared to that of its active state (54 mg per 100ml cf. 125 ml). In his book The Complete Hedgehog, Les Stocker notes that hedgehogs also exhibit a doubling of blood magnesium content and a decrease in body tissue oxygen demand of some 98% (from 550ml per kilogram per hour to only 10ml). Explanations for the aforementioned events have yet to be uncovered, but other species have demonstrated similar increases in magnesium during torpor -- Marvin Riedesel & G. Edgar Folk reported a 50% increase in blood magnesium from two hibernating bat species in a 1956 paper to Nature -- and this element has recently been shown to help prevent hypertension (high blood pressure) and arrhythmia (irregular heart rate) – ergo, the increased magnesium may offer an additional cardioprotective influence
Hedgehogs have evolved a number of physiological strategies that help them cope with the pressures of hibernation. There is a migration of 90% of the white corpuscles to the gastrointestinal tract (presumably to fight any bacterial infections that may arise as food decomposes in the digestive tract) and a significant reduction in the activity of the kidneys and brain (specifically the cerebellum and cerebral cortex). Perhaps the most fascinating adaptation can be seen in the heart. Ordinarily, cold blood returning to the mammalian heart leads to an uncoordinated (often frenzied) contraction of the ventricles, a condition referred to as ventricular fibrillation; this random twitching of the cardiac muscle means that blood isn’t pumped into the systemic circulation and if the arrhythmia continues for more than a few seconds the circulation may collapse. The hedgehog heart has a number of specialised adaptations that help prevent ventricular fibrillation, including reduced adrenergic innervation (few nerves that respond to adrenaline), low noradrenaline content (like adrenaline, noradrenaline is involved in fight-or-flight response and triggers release of glucose from storage), glycogen stores (act as fuel stores) and high alpha-GPDH activity (enzyme pathway that converts fat to energy) – see Nigel Reeve’s Hedgehogs for more details. Despite these protective measures, it is only the peripheral circulation that exhibits a decrease in temperature; the feet, ears and skin are cold to the touch, but the core temperature (e.g. around the heart) is close to normal.
As early as 1925 studies have demonstrated the phenomenon of so-called ‘insulin hibernation’ in several animals -- including dogs, cats and marmots -- following a cold bath (to lower body temperature) and injection with insulin to lower blood sugar levels to a convulsive level. While one could argue the semantics of the term “insulin hibernation” (it’s actually insulin shock, rather than true hibernation), it does demonstrate the possibility for insulin to be involved in the maintenance of hibernation. Indeed, in a 1939 paper from the journal Annales Academiæ Scientiarum Fennicæ, Paavo Suomalainen of Helsinki University demonstrated that injecting hedgehogs with insulin can induce or maintain hibernation. However, several studies have presented evidence that the hibernative state is maintained by the ratio of serotonin and noradrenaline. It appears that when serotonin levels are high, noradrenaline is low and body temperature is decreased causing continuation of hibernation; conversely, when serotonin levels are low and noradrenaline levels are high, body temperature increases and arousal occurs.
It should be mentioned that hibernating hedgehogs aren’t ‘dead to the world’, nor is hibernation a static state. Hibernating hedgehogs will ‘bristle’ (i.e. erect their spines) when touched or exposed to noise, tucking themselves into a tighter ball. Moreover, hibernation fluctuates in accordance with changing environmental conditions and is punctuated by frequent bouts of arousal; undisturbed individuals tend to ‘wake up’ on average every seven to eleven days, although others may not do so for several months. In his New Hedgehog Book, Pat Morris states that it takes three or four hours to raise the body temperature by 25oC (45oF). During these brief (two or three day) intermissions from hibernation the hog may remain in the nest or venture outside. The reasons for these brief periods of activity haven’t been conclusively demonstrated, although suggestions include searching for food to top up fat reserves and removal of metabolic by-products that can only be neutralised in a hyperthermic state. However, in extremely cold weather food is likely to be scarce (hence the need for hibernation in the first place) and there are no data to suggest that either urea or lactate accumulate during hibernation. Nonetheless, even hedgehogs kept under constant conditions in a laboratory arouse periodically -- some 20 times during the course of the winter -- spending only 80% of their hibernation in a hypothermic state; this suggests that periodic arousals are a necessary part of hibernation.
Hedgehogs often use these periods of activity to move nests. Indeed, moving nests during the winter is apparently a common behaviour; in his Hedgehogs book, Nigel Reeve reports how new nests are built throughout the winter and that the occupancy of winter nests varies considerably, with the average nest being occupied for only two months (the maximum was six months). Pat Morris affirms Dr. Reeve’s observations, in a response to the “Q&A…” section of April 2006’s issue of BBC Wildlife Magazine in which he writes: “Hedgehogs rarely stay in the same nest for the whole of the winter – they tend to move and build at least one new nest between November and March. Heavy rain or disturbance of the nest by other animals or humans may force them to move away, but even in constant conditions in the laboratory, winter arousal is normal and frequent.” Similarly, moving nests may be necessary if the temperature falls too low. If exposed to temperature below 1oC (34oF), hedgehogs are vulnerable to frostbite or can even freeze solid. Consequently, brief periods of arousal during exceptionally cold spells may prevent the hedgehog from freezing to death.
Final arousal seems to be triggered by an increasing photoperiod (i.e. the number of light hours in the day starts to increase) and a rise in ambient temperature, although population studies on European hedgehogs have demonstrated a sex biased arousal and hibernation. During his studies on hogs in London, Nigel Reeve found that males were caught during March, while females were rarely caught before May. Dr. Reeve proposed that males may arouse earlier than females in order to gain access to females as soon as they become active (early litters stand a better chance of survival than late ones) or because arousing early allows them to feed with reduced competition and make up for the time spent courting and mating (valuable feeding time). Off-hand, both seem entirely plausible, especially given that Dr. Reeve’s tracking studies have also demonstrated that males range less in these first weeks post-arousal than during the rest of the year (especially during the rut), which may help offset the energy costs associated with early arousal.
The difference in arousal times may be mediated by different controlling factors between the sexes. In his 1986 contribution to Elsevier’s Living in the Cold: Physiological & Biochemical Adaptations, Michel Saboureau demonstrated that a decrease in testosterone caused males to enter hibernation, while the hormone’s absence extended toporic events. In January, as photoperiod begins to increase, males experience a decrease in levels of 5-methoxy-N-acetyltryptamine (commonly known as melatonin, a neurohormone produced by several tissues including the brain’s pineal gland). Melatonin has numerous effects on the body, but in male hedgehogs its decline leads to a rise in testosterone levels, which causes a progressive reactivation of the gonads. So, hibernation in male hedgehogs appears to be heavily influenced by hormonal changes, while -- as Nigel Reeve notes in his book Hedgehogs -- hibernation of females is more closely associated with ambient temperature and food availability than changes in reproductive hormones.
Despite the various suggestions, there is currently no single theory proven to explain the arousal from hibernation, probably because more than one mechanism is involved. Still, it is perhaps difficult to see how changing photoperiods affect hedgehogs deep within their hibernaculums. It has been suggested that hogs could possibly ‘sample’ the photoperiod during their periodic arousals – presumably females also ‘sample’ the food availability and ambient temperature during these ‘intermissions’. Moreover, data from studies by Profs Saboureau, Racey and Fowler show that administration of melatonin in September leads to the onset of testicular reactivation during the Spring, suggesting that it may act as some form of internal ‘timer’ that influences the Spring arousal of males. Thus, an internal timer, food availability and changes in ambient temperature may combine to stimulate the arousal of hedgehogs from hibernation.
During hibernation, it is the WAT that fuels the hedgehog’s metabolism. The BAT is activated upon arousal; this is possible because BAT produces a considerable amount of energy as a by-product of its respiration (as much as 400 watts per kilogram of tissue). All biological tissues produce heat as a by-product of respiration, but this is typically negligible. In WAT, the final step of cellular respiration that the fatty acids go through is a biochemical process known as oxidative phosphorylation; in this process, adenosine triphosphate (ATP, the energy source for virtually all cellular functions) is created. In the case of BAT, this last step is prevented by a mitochondrial uncoupling protein (UCP) that effectively ‘short circuits’ the oxidative phosphorylation process, allowing the oxidation of fatty acids to produce heat instead of ATP. This process enables a substantial amount of heat to be generated (about twenty-times that of WAT), without the reliance on spasmodic reflex muscle contraction (i.e. shivering); hence this process is often referred to as “non-shivering thermogenesis”. According to Dr. Reeve (Hedgehogs), the thermostatic control of BAT is achieved by sensors in the hypothalamus, skin and along the spinal cord, while its metabolism is controlled by the sympathetic (i.e. those responsible for increasing or decreasing a mechanism/response) nerve endings that penetrate the tissue and by circulating adrenal hormones.
In a laboratory setting, arousal can take as little as two hours; under more natural conditions Paul Racey and Paul Fowler found that it took 12 hours for their subjects to become fully active – BAT can warm the body at between 6oC (11oF) and 21oC (38oF) per hour depending on the individual and ambient conditions. In Hedgehogs, Nigel Reeve describes the arousal process. Upon arousal, BAT is metabolised and the heart beats vigorously (heart rate may increase from 10 to 300 bpm) circulating the heat throughout the hedgehog’s body (the BAT is infiltrated by a rich network of capillaries which supply it with oxygen to fuel respiration and help distribute the heat). As the body temperature rises past 15oC (59oF), carbohydrate metabolism resumes and at 20oC (68oF) glucagon (a pancreatic hormone) secretion rises, stimulating the release of glucose into the bloodstream. The eyes remain closed below approximately 20oC; above this temperature the eyes open and the front of the body may stand and shiver. When the body temperature has increased to between 28oC and 30oC (82 – 84oF) the hog begins to move around and when normal body temperature is reached (i.e. ~ 35oC / 95oF), the hedgehog is fully active. Studies on captive individuals suggest that hedgehogs lose one or two grams of body weight (0.2 to 0.3%) per day while in hibernation and thus, by the time the hedgehog is fully aroused, it needs to eat and drink as a matter or priority. Weight loss varies geographically, but the hog may have lost anywhere from 25% (in the UK) to 40% (in Finland) of its pre-hibernation body weight. Hence, a pre-hibernation weight of about 700 grams (1 ½ lbs.) is recommended by most vets and hedgehog welfare charities.
Fri Jan 06, 2012 3:47 pm
