Hibernation

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Northern bat hibernating in Norway

Hibernation (from Latin: hībernus, of winter) is a suppressed metabolic state that falls under the umbrella-term of torpor or dormancy. It is but one of many forms of metabolic suppression. Hibernation is a widespread and common survival strategy expressed under the threat of a metabolic energy crisis. Conversely and considering that some animals exist in this state for the greater part of the year, it could just as easily be considered the default metabolic state and up-regulation of metabolism merely a response to the availability of energy. As the name suggests, hibernation has a seasonal connotation that points to triggering by the threat of lowered ambient temperatures, famine, and darkness, e.g., autumn and winter; hibernation during the summer months is called aestivation. Some reptile species (ectotherms) are said to brumate, or undergo brumation. For some animals it is not possible to maintain, let alone raise metabolic rate to concurrently cope with cold and famine, hence they suppress metabolism and "sit it out" until conditions improve.

Attempts at defining or triggering hibernation have, however, proved elusive. For example, merely exposing animals that hibernate to cold does not always trigger hibernation. Instead it may trigger hypothermia, a life-threatening pathologic condition. In addition, the duration for which an animal must remain in torpor for it to be qualified as a hibernator remains debatable. Depending on the species, its size, environmental trigger (e.g., ambient temperature, light levels, etc.), time of year, body condition, and fat stores, hibernation could arguably last as short as a day or less, or many months. The longest reported hibernation bout on record in a mammal, a marsupial, is just over a year. Additional difficulty in defining hibernation comes by way of the fact that small mammals frequently arouse during hibernation. Unequivocally, however, torpid states, whatever the metabolic energy threat, are fundamentally typified by lowered core-body temperatures, prolonged pauses between breaths and lowered heart rates, i.e., to values below those of so-called basal metabolic rate (BMR). Even here though, it remains unclear what degree of suppression is required to be classified as hibernation, especially considering that the scope for metabolic suppression scales inversely with body mass, and large animals, because of an already lowered basal metabolic rate, are closer to universal minimum metabolic rate (UMMR), a rate found to be fundamentally invariant in animals ranging in size from bacteria to blue whales. In fact, bears were not considered true hibernators by many, for a long time, because they needed only to suppress their metabolism and temperature by modest amounts to enter deep hibernation.

Often associated with lowered ambient temperatures, the central function of hibernation is to ensure survival by conserving energy in anticipation of a period of food shortage. The down-regulation of metabolism lowers metabolic needs and enhances tolerance of cold. To achieve this energy saving state, endotherms entrain a series of energy-conserving physiologic response, like peripheral vasoconstriction, bradycardia, lowered respiratory needs, core-body cooling, etc. This has the concurrent effect of lowering whole-body metabolic rate, by effectively isolating central and more `vital´ tissues from peripheral tissues and letting the periphery cool. In this stage, core (visceral) temperature may remains stable; it remains undetermined whether visceral temperature reflects brain temperature.

Typically animals that enter prolonged and uninterrupted torpid bouts, like seasonal hibernation, prepare for hibernation by storing body-fat on which to live. Larger species become hyperphagic and eat a large amount of food and store the energy in fat deposits. In smaller species, in which low core-body temperatures require frequent rewarming arousals, an energetically-expensive exercise, and whose body-fat storing capacity is very limited, food caching replaces body-fat stores.[1] Some species of mammals hibernate while gestating young, which are either born while the mother hibernates or shortly afterwards.[2]

Hibernating mammals[edit]

Rodents[edit]

Hibernation among rodents has been extensively studied for centuries. Species of ground squirrel, marmot, prairie dog, dormouse, and hamster have all been shown to demonstrate hibernation. These animals all exhibit the classic hibernation pattern where body temperature remains at ambient for days to weeks, followed by a brief (<24hr) return to higher body temperature. The ability to cool down scales inversely with body size.

Primates[edit]

While hibernation has long been studied in rodents, namely ground squirrels, no primate or tropical mammal was known to hibernate prior to the discovery that the fat-tailed dwarf lemur of Madagascar hibernates in tree holes for seven months of the year.[3] Malagasy winter temperatures sometimes rise to over 30 °C (86 °F), so hibernation is not exclusively an adaptation to low ambient temperatures. The hibernation of this lemur is strongly dependent on the thermal behaviour of its tree hole: if the hole is poorly insulated, the lemur's body temperature fluctuates widely, passively following the ambient temperature; if well insulated, the body temperature stays fairly constant and the animal undergoes regular spells of arousal.[4] Dausmann found that hypometabolism in hibernating animals is not necessarily coupled to a low body temperature.[5][citation needed]

Bears[edit]

For many decades it remained controversial whether bears actually hibernated, because over-wintering bears only experienced a modest drop in core-body temperature compared to smaller animals. What defines hibernation, however, is not the degree of temperature reduction, but the metabolic suppression. (Adult) human-sized bears can, however, lower (aerobic) metabolic rate to some 75% below, so-called, basal metabolic rates, which indicates that bears are hibernators. Indeed, northern-most bears will neither eat nor drink for periods as long as 8 months, relying only on stored body-fat reserves for energy and water. Though it is believed that bear hibernation is very different from either rodent or primate hibernation and involves temperature-independent metabolic suppression, because the modest decreases in core temperature do not account for the large decrease in metabolic rate, this belief does not consider the effect of metabolic reductions that can occur through extensive peripheral vasoconstriction. For example, it is known that peripheral tissues contribute as much as 50% to metabolism. This discrepancy alone would be sufficient to account for the `missing´ proportion and without having to resort to more esoteric physiologic mechanism. This effect has been observed in other torpid metabolic states, like diving. In diving penguins and seals, for example, metabolic rate can be lowered without resorting to any core (visceral) temperature decreases merely through extensive vasoconstriction of peripheral tissue beds.

They are able to recycle their proteins and urine, allowing them to both stop urinating for months and stop muscle atrophy.[6][7]

Obligate hibernators[edit]

Obligate hibernators are defined as animals that spontaneously, and annually, enter hibernation regardless of ambient temperature and access to food. Obligate hibernators include many species of ground squirrels, other rodents, mouse lemurs, the European hedgehog and other insectivores, monotremes, marsupials, and even butterflies such as the small tortoiseshell.[8] These undergo what has been traditionally called "hibernation": the physiological state where the body temperature drops to near ambient (environmental) temperature, and heart and respiration rates slow drastically. The typical winter season for these hibernators is characterized by periods of torpor interrupted by periodic, euthermic arousals, wherein body temperatures and heart rates are restored to euthermic (more typical) levels. The cause and purpose of these arousals is still not clear.

The question of why hibernators may experience the periodic arousals (returns to high body temperature) has plagued researchers for decades, and while there is still no clear cut explanation, there are a myriad of hypotheses on the topic. One favored hypothesis is that hibernators build a 'sleep debt' during hibernation, and so must occasionally warm up in order to sleep. This has been supported by evidence in the arctic ground squirrel.[9] Another theory states that the brief periods of high body temperature during hibernation are used by the animal to restore its available energy sources.[10] Yet another theory states that the frequent returns to high body temperature allow mammals to initiate an immune response.[11]

Hibernating arctic ground squirrels may exhibit abdominal temperatures as low as -2.9 °C, maintaining sub-zero abdominal temperatures for more than three weeks at a time, although the temperatures at the head and neck remain at 0 ˚C or above.[12]

Historically there was a question of whether or not bears truly hibernate, since they experience only a modest decline in body temperature (3-5°C) compared with what other hibernators undergo (32°C+). Many researchers thought that their deep sleep was not comparable with true, deep hibernation. This theory has been refuted by recent research in captive black bears.[13]

Black bear mother and cubs "denning"

Facultative hibernation[edit]

Unlike obligate hibernators, facultative hibernators only enter hibernation when either cold stressed or food deprived, or both. A good example of the differences between the two types of hibernation can be seen among the prairie dogs; where the white-tailed prairie dog is an obligate hibernator and the closely related black-tailed prairie dog is a facultative hibernator.[14]

Hibernating birds[edit]

Historically, Pliny the Elder believed swallows hibernated, and ornithologist Gilbert White pointed to anecdotal evidence in The Natural History of Selborne that indicated as much. Birds typically do not hibernate, instead utilizing torpor. One known exception is the common poorwill (Phalaenoptilus nuttallii), first documented by Edmund Jaeger.[15][16]

Dormancy in fish[edit]

Fish are ectothermic, and so, by definition, cannot hibernate because they cannot actively down-regulate their body temperature or their metabolic rate. However, they can experience decreased metabolic rates associated with colder environments and/or low oxygen availability (hypoxia) and can experience dormancy. For a couple of generations[vague] during the 20th century it was thought that basking sharks settled to the floor of the North Sea and became dormant. Research by Dr David Sims in 2003 dispelled this hypothesis,[17] showing that the sharks actively traveled huge distances throughout the seasons, tracking the areas with the highest quantity of plankton. The epaulette sharks have been documented to be able to survive for long periods of time without oxygen, even being left high and dry, and at temperatures of up to 26 °C (79 °F).[18] Other animals able to survive long periods without oxygen include the goldfish, the red-eared slider turtle, the wood frog, and the bar-headed goose.[19] However, the ability to survive hypoxic or anoxic conditions is not the same, nor closely related, to endotherm hibernation.

Hibernation induction trigger[edit]

Hibernation induction trigger (HIT) is a bit of misnomer. Although research in the 1990s hinted at the ability to induce torpor in animals by injection of blood taken from a hibernating animal, further research has been unable to reproduce this phenomenon. Despite the inability to induce torpor, there are substances in hibernator blood that can lend protection to organs for possible transplant. Researchers were able to prolong the life of an isolated pig's heart with a HIT.[20] This may have potentially important implications for organ transplant, as it could allow organs to survive for up to 18 or more hours, outside the human body. This would be a great improvement from the current 6 hours.

This supposed HIT is a mixture derived from serum, including at least one opioid-like substance. DADLE is an opioid that in some experiments has been shown to have similar functional properties.[21]

Human (artificial) hibernation[edit]

To date, no dimmer- or master-switch to trigger this state connected to the physical environment has been found in any animal, let alone any human. Nonetheless, animals seem to enter hibernation based on environmental cues. Research groups looking to identify a means to trigger or mimic this state are, with the exception of one private venture (Hibernaut), academic groups, by and large located in the United States (e.g., University of Alaska, Fairbanks; Oregon State University; Duke University, University of Minnesota). Hibernaut stands unique because it is the first and only study to attempt to trigger metabolic suppression in a human; all other experimental trials to date have involved rodents. Though it is a fundamental tenet of biology and medicine that humans are considered incapable of lowering core temperature (anapyrexia), except pathologically (e.g., hypothermia), this first-in-human experiment was able to trigger on-demand metabolic suppression (brain cooling) by as much as ca. 4 degrees in about a dozen minutes, and without the use of artificial drugs or an `ice-cubes´ approach. This is an important milestone because brain cooling would be considered a critical hallmark for potentially triggering a deep, sustained and neuroprotective form this state in humans. Attempts at seeing how low the dimmer-switch goes and how long it can be sustained are planned in 2014. It remains to be seen if this state will result in suspended animation and what specific benefits this metabolic state will confer.

The ability for humans to hibernate would be useful for a number of reasons, of which neuroprotection is central, especially medical emergencies. Other benefits include:

Hibernation, and the species that are able to utilize it, have become fantastic models for many different human diseases. Hibernators make natural models for stroke, ischemia-reperfusion injury, diabetes, obesity, and depression.[22][23][24][25]

See also[edit]

References[edit]

  1. ^ Humphries, M. M.; Thomas, D.W., Kramer, D.L. (2003). "The role of energy availability in mammalian hibernation: A cost-benefit approach". Physiological and Biochemical Zoology 76 (2): 165–179. 
  2. ^ Hellgren, Eric C. (1998). "Physiology of Hibernation in Bears". Ursus 10: 467–477. JSTOR 3873159. 
  3. ^ Dausmann, K.H.; Glos, J., Ganzhorn, J.U., Heldmaier, G. (2005). "Hibernation in the tropics: lessons from a primate". Comparative Physiology B 175 (3): 147–155. doi:10.1007/s00360-004-0470-0. 
  4. ^ Blanco, M. B.; Dausmann, K.; Ranaivoarisoa, J. F.; Yoder, A. D. (2013). "Underground Hibernation in a Primate". Scientific Reports. doi:10.1038/srep01768. 
  5. ^ 429 (6994) http://www.nature.com/nature/journal/v429/n6994/full/429825a.html?lang=en.  Missing or empty |title= (help)
  6. ^ Lundberg, D.A.; Nelson, R.A., Wahner, H.W., Jones, J.D. (1976). "Protein metabolism in the black bear before and during hibernation". Mayo Clinnic Proceedings 51 (11): 716–722. 
  7. ^ Nelson, R.A. (1980). "Protein and fat metabolism in hibernating bears". FASEB J. 39 (12): 2955–2958. PMID 6998737. 
  8. ^ Territorial Behaviour of the Nymphalid Butterflies, Aglais urticae (L.) and Inachis io (L.) R. R. Baker Journal of Animal Ecology , Vol. 41, No. 2 (Jun., 1972), pp. 453-469
  9. ^ Daan S, Barnes BM, Strijkstra AM (1991). "Warming up for sleep? Ground squirrels sleep during arousals from hibernation". Neurosci. Lett. 128 (2): 265–8. doi:10.1016/0304-3940(91)90276-Y. PMID 1945046. 
  10. ^ Galster, W.; Morrison, P.R. (1975). "Gluconeogenesis in arctic ground squirrels between periods of hibernation". American Journal of Physiology 228 (1): 325–330. 
  11. ^ Prendergast, B.J.; Freeman, D.A., Zucker, I., Nelson, R.J. (2002). "Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels". AJP - Regu. Physiol. 282 (4): R1054–R1062. doi:10.1152/ajpregu.00562.2001. PMID 11893609. 
  12. ^ Barnes, Brian M. (30 June 1989). "Freeze Avoidance in a Mammal: Body Temperatures Below 0 °C in an Arctic Hibernator" (PDF). Science (American Association for the Advancement of Science) 244 (4912): –1616. doi:10.1126/science.2740905. PMID 2740905. Retrieved 2008-11-23. 
  13. ^ Toien, Oivind; Black, J., Edgar, D.M., Grahn, D.A., Heller, H.C., Barnes, B.M. (February 2011). "Black Bears: Independence of Metabolic Suppression from temperature". Science 331 (6019): 906–909. doi:10.1126/science.1199435. PMID 21330544. 
  14. ^ Harlow, H.J.; Frank, C.L. (2001). "The role of dietary fatty acids in the evolution of spontaneous and facultative hibernation patterns in prairie dogs". J. Comp. Physiol. B. 171: 77–84. 
  15. ^ Jaeger, Edmund C. (May–June 1949). "Further Observations on the Hibernation of the Poor-will". The Condor. 3 51: 105–109. JSTOR 1365104. "Earlier I gave an account (Condor, 50, 1948:45) of the behavior of a Poor-will (Phalaenoptilus nuttallinii) which I found in a state of profound torpidity in the winter of 1946-47 in the Chuckawalla Mountains of the Colorado Desert, California." 
  16. ^ McKechnie, Andrew W.; Ashdown, Robert A. M., Christian, Murray B. & Brigham, R. Mark. "Torpor in an African caprimulgid, the freckled nightjar Caprimulgus tristigma". Journal of Avian Biology 38 (3): 261–266. doi:10.1111/j.2007.0908-8857.04116.x. 
  17. ^ "Seasonal movements and behavior of basking sharks from archival tagging". Marine Ecology Progress Series (248): 187–196. 2003. 
  18. ^ "A Shark With an Amazing Party Trick". New Scientist 177 (2385): 46. 8 March 2003. Retrieved 2006-10-06. 
  19. ^ Breathless: A shark with an amazing party trick is teaching doctors how to protect the brains of stroke patients. Douglas Fox, New Scientist vol 177 issue 2385 - 8 March 2003, page 46. Last accessed November 9, 2006.
  20. ^ Bolling, S.F.; Tramontini, N.L., Kilgore, K.S., Su, T-P., Oeltgen, P.R., Harlow, H.H. (1997). "Use of "Natural" Hibernation Induction Triggers for Myocardial Protection". The Annals of Thoracic Surgery 64 (3): 623–627. 
  21. ^ Oeltgen PR, Nilekani SP, Nuchols PA, Spurrier WA, Su TP (1988). "Further studies on opioids and hibernation: delta opioid receptor ligand selectively induced hibernation in summer-active ground squirrels". Life Sc. 43 (19): 1565–74. doi:10.1016/0024-3205(88)90406-7. PMID 2904105. 
  22. ^ Drew, K; et al. (2001). "Neuroprotective adaptations in hibernation: therapeutic implications for ischemia-reperfusion, traumatic brain injury and neurodegenerative diseases". Free Radical Biology & Medicine 31 (5): 563–573. 
  23. ^ Martin, S.L. (2005). "Mammalian hibernation: a naturally reversible model for insulin resistance in man?". Diabetes and Vascular Research 5 (2): 76–81. 
  24. ^ Boyer, B.B.; et al. (1997). "Leptin prevents posthibernation weight gain but does not reduce energy expenditure in arctic ground squirrels.". Comp. Biochem. and Physiol. Part C 118 (3): 405–412. 
  25. ^ Tsiouris, J.A. (2005). "Metabolic depression in hibernation and major depression: An explanatory theory and an animal model of depression". Medical Hypotheses 65: 829–840. 

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