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Torpor

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Animal dormancy

Torpor is a state of decreased physiological activity in an animal, usually marked by a reduced body temperature and metabolic rate. Torpor enables animals to survive periods of reduced food availability.[1] The term "torpor" can refer to the time a hibernator spends at low body temperature, lasting days to weeks, or it can refer to a period of low body temperature and metabolism lasting less than 24 hours, as in "daily torpor".

Animals that undergo daily torpor include birds (even tiny hummingbirds, notably Cypselomorphae)[2][3] and some mammals, including many marsupial species,[4][5] rodent species (such as mice), and bats.[6] During the active part of their day, such animals maintain normal body temperature and activity levels, but their metabolic rate and body temperature drop during a portion of the day (usually night) to conserve energy.[citation needed]

Some animals seasonally go into long periods of inactivity, with reduced body temperature and metabolism, made up of multiple bouts of torpor. This is known as hibernation if it occurs during winter or aestivation if it occurs during the summer. Daily torpor, on the other hand, is not seasonally dependent and can be an important part of energy conservation at any time of year.[7]

Torpor is a well-controlled thermoregulatory process and not, as previously thought, the result of switching off thermoregulation.[8] Marsupial torpor differs from non-marsupial mammalian (eutherian) torpor in the characteristics of arousal. Eutherian arousal relies on a heat-producing brown adipose tissue as a mechanism to accelerate rewarming. The mechanism of marsupial arousal is unknown, but appears not to rely on brown adipose tissue.[9]

Evolution

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The evolution of torpor likely accompanied the development of homeothermy.[10] Animals capable of maintaining a body temperature above ambient temperature when other members of its species would not have a fitness advantage. Benefits of maintaining internal temperatures include increased foraging time and less susceptibility to extreme drops in temperature.[10] This adaptation of increasing body temperature to forage has been observed in small nocturnal mammals when they first wake up in the evening.[11][12][13]

Although homeothermy lends advantages such as increased activity levels, small mammals and birds maintaining an internal body temperature spend up to 100 times more energy in low ambient temperatures compared to ectotherms.[14] To cope with this challenge, these animals maintain a much lower body temperature, staying just over ambient temperature rather than at normal operating temperature. This reduction in body temperature and metabolic rate allows the prolonged survival of animals capable of entering torpid states.

In 2020, scientists reported evidence of the torpor in Lystrosaurus living ~250 Mya in Antarctica – the oldest evidence of a hibernation-like state in a vertebrate animal.[15][16][17]

Functions

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Slowing metabolic rate to conserve energy in times of insufficient resources is the primarily noted purpose of torpor.[18] This conclusion is largely based on laboratory studies where torpor was observed to follow food deprivation.[19] There is evidence for other adaptive functions of torpor where animals are observed in natural contexts:

Circadian rhythm during torpor

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Animals that can enter torpor rely on biological rhythms such as circadian and circannual rhythms to continue natural functions. Different animals will manage their circadian rhythm differently, and in some species it's seen to completely stop (such as in European hamsters). Other organisms, such as a black bear, enter torpor and switch to multi-day cycles rather than rely on a circadian rhythm. However, it is seen that both captive and wild bears express similar circadian rhythms when entering torpor. Bears entering torpor in a simulated den with no light expressed normal but low functioning rhythms. The same was observed in wild bears denning in natural areas. The function of circadian rhythms in black, brown, and polar bears suggest that their system of torpor is evolutionarily advanced.[20]

Energy conservation in small birds

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Anna's hummingbird (Calypte anna) in nocturnal torpor during a cold winter night (−8 °C (18 °F) near Vancouver, British Columbia. The bird remained in torpor with an unchanged position for more than 12 hours.

Torpor has been shown to be a strategy of small migrant birds to preserve their body energy stores.[21][22] Hummingbirds, resting at night during migration, were observed to enter torpor which helped to conserve fat stores during migration or cold nights at high altitude.[19][21][22]

This strategy of using torpor to preserve energy stores, such as fat, has also been observed in wintering chickadees.[23] Black-capped chickadees, living in temperate forests of North America, do not migrate south during winter. The chickadee can maintain a body temperature 12 °C lower than normal. This reduction in metabolism allows it to conserve 30% of fat stores amassed from the previous day.[23]

Advantage in environments with unpredictable food sources

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Torpor can be a strategy of animals with unpredictable food supplies.[24] For example, high-latitude living rodents use torpor seasonally when not reproducing. These rodents use torpor as means to survive winter and live to reproduce in the next reproduction cycle when food sources are plentiful, separating periods of torpor from the reproduction period. The eastern long-eared bat uses torpor during winter and is able to arouse and forage during warm periods.[25] Some animals use torpor during their reproductive cycle, as seen in unpredictable habitats.[24] They experience the cost of a prolonged reproduction period but the payoff is survival to be able to reproduce at all.[24]

Survival during mass extinctions

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It is suggested that this daily torpor use may have allowed survival through mass extinction events.[26] Heterotherms make up only four out of 61 mammals confirmed to have gone extinct over the last 500 years.[26] Torpor enables animals to reduce energy requirements allowing them to better survive harsh conditions.

Inter-species competition

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Interspecific competition occurs when two species require the same resource for energy production.[27] Torpor increases fitness in the case of inter-specific competition with the nocturnal common spiny mouse.[27] When the golden spiny mouse experiences reduced food availability by diet overlap with the common spiny mouse it spends more time in a torpid state.

Parasite resistance by bats

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A drop in temperature from torpor has been shown to reduce the ability of parasites to reproduce.[28] In temperate zones, the reproductive rates of ectoparasites on bats decrease when the bats enter torpor. In regions where bats don't undergo torpor, the parasites maintain a consistent reproductive rate throughout the year.

NASA deep sleep option for a mission to Mars

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In 2013, SpaceWorks Engineering began researching a way to dramatically cut the cost of a human expedition to Mars by putting the crew in extended torpor for 90 to 180 days. Traveling while hibernating would reduce astronauts' metabolic functions and minimize requirements for life support during multi-year missions.[29]

See also

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Notes

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  1. ^ Vuarin, Pauline; Dammhahn, Melanie; Kappeler, Peter M.; Henry, Pierre-Yves (September 2015). "When to initiate torpor use? Food availability times the transition to winter phenotype in a tropical heterotherm" (PDF). Oecologia. 179 (1): 43–53. Bibcode:2015Oecol.179...43V. doi:10.1007/s00442-015-3328-0. PMID 25953115. S2CID 17050304.
  2. ^ Hainsworth, F. R.; Wolf, L. L. (17 April 1970). "Regulation of Oxygen Consumption and Body Temperature during Torpor in a Hummingbird, Eulampis jugularls". Science. 168 (3929): 368–369. Bibcode:1970Sci...168..368R. doi:10.1126/science.168.3929.368. PMID 5435893. S2CID 30793291.
  3. ^ "Hummingbirds". Migratory Bird Center, Smithsonian National Zoological Park. Archived from the original on 2008-02-14.
  4. ^ Geiser, F (1994). "Hibernation and Daily Torpor in Marsupials - a Review". Australian Journal of Zoology. 42 (1): 1. doi:10.1071/zo9940001. S2CID 84914662.
  5. ^ Stannard, H.J.; Fabian, M.; Old, J.M. (2015). "To bask or not to bask: Behavioural thermoregulation in two species of dasyurid, Phascogale calura and Antechinomys laniger". Journal of Thermal Biology. 53: 66–71. Bibcode:2015JTBio..53...66S. doi:10.1016/j.jtherbio.2015.08.012. PMID 26590457.
  6. ^ Bartels, W.; Law, B. S.; Geiser, F. (7 April 1998). "Daily torpor and energetics in a tropical mammal, the northern blossom-bat Macroglossus minimus (Megachiroptera)". Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology. 168 (3): 233–239. doi:10.1007/s003600050141. PMID 9591364. S2CID 16870476.
  7. ^ "Wikipedia, the free encyclopedia". www.wikipedia.org. Retrieved 2024-03-22.
  8. ^ Geiser, Fritz (March 2004). "Metabolic Rate and Body Temperature Reduction During Hibernation and Daily Torpor". Annual Review of Physiology. 66 (1): 239–274. doi:10.1146/annurev.physiol.66.032102.115105. PMID 14977403. S2CID 22397415.
  9. ^ Dawson, T. J.; Finch, E.; Freedman, L.; Hume, I. D.; Renfree, Marilyn; Temple-Smith, P. D. "Morphology and Physiology of the Metatheria" (PDF). In Walton, D. W.; Richardson, B. J. (eds.). Fauna of Australia - Volume 1B Mammalia. ISBN 978-0-644-06056-1.
  10. ^ a b Geiser, Fritz; Stawski, Clare; Wacker, Chris B.; Nowack, Julia (2 November 2017). "Phoenix from the Ashes: Fire, Torpor, and the Evolution of Mammalian Endothermy". Frontiers in Physiology. 8: 842. doi:10.3389/fphys.2017.00842. PMC 5673639. PMID 29163191.
  11. ^ Stawski, Clare; Geiser, Fritz (January 2010). "Fat and fed: frequent use of summer torpor in a subtropical bat". Naturwissenschaften. 97 (1): 29–35. Bibcode:2010NW.....97...29S. doi:10.1007/s00114-009-0606-x. PMID 19756460. S2CID 9499097.
  12. ^ Warnecke, Lisa; Turner, James M.; Geiser, Fritz (29 November 2007). "Torpor and basking in a small arid zone marsupial". Naturwissenschaften. 95 (1): 73–78. Bibcode:2008NW.....95...73W. doi:10.1007/s00114-007-0293-4. PMID 17684718. S2CID 21993888.
  13. ^ Körtner, Gerhard; Geiser, Fritz (April 2009). "The key to winter survival: daily torpor in a small arid-zone marsupial". Naturwissenschaften. 96 (4): 525–530. Bibcode:2009NW.....96..525K. doi:10.1007/s00114-008-0492-7. PMID 19082573. S2CID 3093539.
  14. ^ Bartholomew, George A. (1982). "Energy Metabolism". In Gordon, Malcolm S. (ed.). Animal Physiology: Principles and Adaptations. Macmillan. pp. 46–93. ISBN 978-0-02-345320-5.
  15. ^ "Fossil evidence of 'hibernation-like' state in 250-million-year-old Antarctic animal". phys.org. Retrieved 7 September 2020.
  16. ^ "Fossil suggests animals have been hibernating for 250 million years". UPI. Retrieved 7 September 2020.
  17. ^ Whitney, Megan R.; Sidor, Christian A. (December 2020). "Evidence of torpor in the tusks of Lystrosaurus from the Early Triassic of Antarctica". Communications Biology. 3 (1): 471. doi:10.1038/s42003-020-01207-6. PMC 7453012. PMID 32855434.
  18. ^ Allaby, Michael (2014). A Dictionary of Zoology. Oxford University Press. p. 963. ISBN 9780199684274.
  19. ^ a b Carpenter, F. Lynn; Hixon, Mark A. (May 1988). "A new function for torpor: Fat conservation in a wild migrant hummingbird". The Condor. 90 (2): 373–378. doi:10.2307/1368565. JSTOR 1368565.
  20. ^ Jansen, Heiko T.; Leise, Tanya; Stenhouse, Gordon; Pigeon, Karine; Kasworm, Wayne; Teisberg, Justin; Radandt, Thomas; Dallmann, Robert; Brown, Steven; Robbins, Charles T. (December 2016). "The bear circadian clock doesn't 'sleep' during winter dormancy". Frontiers in Zoology. 13 (1): 42. doi:10.1186/s12983-016-0173-x. PMC 5026772. PMID 27660641. ProQuest 1825614860.
  21. ^ a b Wolf, Blair O.; McKechnie, Andrew E.; Schmitt, C. Jonathan; Czenze, Zenon J.; Johnson, Andrew B.; Witt, Christopher C. (2020). "Extreme and variable torpor among high-elevation Andean hummingbird species". Biology Letters. 16 (9): 20200428. doi:10.1098/rsbl.2020.0428. ISSN 1744-9561. PMC 7532710. PMID 32898456.
  22. ^ a b Greenwood, Veronique (2020-09-08). "These hummingbirds take extreme naps. Some may even hibernate". The New York Times. ISSN 0362-4331. Retrieved 2020-09-09.
  23. ^ a b Chaplin, Susan Budd (1974). "Daily energetics of the black-capped chickadee, Parus atricapillus, in winter". Journal of Comparative Physiology. 89 (4): 321–330. doi:10.1007/BF00695350. S2CID 34190772.
  24. ^ a b c McAllan, B. M.; Geiser, F. (1 September 2014). "Torpor during Reproduction in Mammals and Birds: Dealing with an Energetic Conundrum". Integrative and Comparative Biology. 54 (3): 516–532. doi:10.1093/icb/icu093. PMID 24973362.
  25. ^ Stawski, Clare; Turbill, Christopher; Geiser, Fritz (May 2009). "Hibernation by a free-ranging subtropical bat (Nyctophilus bifax)". Journal of Comparative Physiology B. 179 (4): 433–441. doi:10.1007/s00360-008-0328-y. PMID 19112568. S2CID 20283021.
  26. ^ a b Geiser, Fritz; Brigham, R. Mark (2012). "The Other Functions of Torpor". Living in a Seasonal World. pp. 109–121. doi:10.1007/978-3-642-28678-0_10. ISBN 978-3-642-28677-3.
  27. ^ a b Levy, O.; Dayan, T.; Kronfeld-Schor, N. (1 September 2011). "Interspecific Competition and Torpor in Golden Spiny Mice: Two Sides of the Energy-Acquisition Coin". Integrative and Comparative Biology. 51 (3): 441–448. doi:10.1093/icb/icr071. PMID 21719432.
  28. ^ Lourenço, Sofia; Palmeirim, Jorge Mestre (December 2008). "Which factors regulate the reproduction of ectoparasites of temperate-zone cave-dwelling bats?". Parasitology Research. 104 (1): 127–134. doi:10.1007/s00436-008-1170-6. PMID 18779978. S2CID 24822087.
  29. ^ Hall, Loura (19 July 2013). "Torpor Inducing Transfer Habitat For Human Stasis To Mars". NASA. Retrieved 20 March 2018.
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