Torpor

Last updated

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".

Contents

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

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

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

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

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

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

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

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

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

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

Notes

  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. 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. 1 2 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. 1 2 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. 1 2 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. 1 2 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. 1 2 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. 1 2 3 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. 1 2 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. 1 2 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.

Related Research Articles

<span class="mw-page-title-main">Sugar glider</span> Species of Australian marsupial

The sugar glider is a small, omnivorous, arboreal, and nocturnal gliding possum. The common name refers to its predilection for sugary foods such as sap and nectar and its ability to glide through the air, much like a flying squirrel. They have very similar habits and appearance to the flying squirrel, despite not being closely related—an example of convergent evolution. The scientific name, Petaurus breviceps, translates from Latin as "short-headed rope-dancer", a reference to their canopy acrobatics.

<span class="mw-page-title-main">Circadian rhythm</span> Natural internal process that regulates the sleep-wake cycle

A circadian rhythm, or circadian cycle, is a natural oscillation that repeats roughly every 24 hours. Circadian rhythms can refer to any process that originates within an organism and responds to the environment. Circadian rhythms are regulated by a circadian clock whose primary function is to rhythmically co-ordinate biological processes so they occur at the correct time to maximise the fitness of an individual. Circadian rhythms have been widely observed in animals, plants, fungi and cyanobacteria and there is evidence that they evolved independently in each of these kingdoms of life.

<span class="mw-page-title-main">Hummingbird</span> Family of birds

Hummingbirds are birds native to the Americas and comprise the biological family Trochilidae. With approximately 366 species and 113 genera, they occur from Alaska to Tierra del Fuego, but most species are found in Central and South America. As of 2024, 21 hummingbird species are listed as endangered or critically endangered, with numerous species declining in population.

<span class="mw-page-title-main">Hibernation</span> Physiological state of dormant inactivity in order to pass the winter season

Hibernation is a state of minimal activity and metabolic depression undergone by some animal species. Hibernation is a seasonal heterothermy characterized by low body-temperature, slow breathing and heart-rate, and low metabolic rate. It most commonly occurs during winter months.

<span class="mw-page-title-main">Dormancy</span> State of minimized physical activity of an organism

Dormancy is a period in an organism's life cycle when growth, development, and physical activity are temporarily stopped. This minimizes metabolic activity and therefore helps an organism to conserve energy. Dormancy tends to be closely associated with environmental conditions. Organisms can synchronize entry to a dormant phase with their environment through predictive or consequential means. Predictive dormancy occurs when an organism enters a dormant phase before the onset of adverse conditions. For example, photoperiod and decreasing temperature are used by many plants to predict the onset of winter. Consequential dormancy occurs when organisms enter a dormant phase after adverse conditions have arisen. This is commonly found in areas with an unpredictable climate. While very sudden changes in conditions may lead to a high mortality rate among animals relying on consequential dormancy, its use can be advantageous, as organisms remain active longer and are therefore able to make greater use of available resources.

<span class="mw-page-title-main">Endotherm</span> Organism that maintains body temperature largely by heat from internal bodily functions

An endotherm is an organism that maintains its body at a metabolically favorable temperature, largely by the use of heat released by its internal bodily functions instead of relying almost purely on ambient heat. Such internally generated heat is mainly an incidental product of the animal's routine metabolism, but under conditions of excessive cold or low activity an endotherm might apply special mechanisms adapted specifically to heat production. Examples include special-function muscular exertion such as shivering, and uncoupled oxidative metabolism, such as within brown adipose tissue.

<span class="mw-page-title-main">Thermoregulation</span> Ability of an organism to keep its body temperature within certain boundaries

Thermoregulation is the ability of an organism to keep its body temperature within certain boundaries, even when the surrounding temperature is very different. A thermoconforming organism, by contrast, simply adopts the surrounding temperature as its own body temperature, thus avoiding the need for internal thermoregulation. The internal thermoregulation process is one aspect of homeostasis: a state of dynamic stability in an organism's internal conditions, maintained far from thermal equilibrium with its environment. If the body is unable to maintain a normal temperature and it increases significantly above normal, a condition known as hyperthermia occurs. Humans may also experience lethal hyperthermia when the wet bulb temperature is sustained above 35 °C (95 °F) for six hours. Work in 2022 established by experiment that a wet-bulb temperature exceeding 30.55°C caused uncompensable heat stress in young, healthy adult humans. The opposite condition, when body temperature decreases below normal levels, is known as hypothermia. It results when the homeostatic control mechanisms of heat within the body malfunction, causing the body to lose heat faster than producing it. Normal body temperature is around 37°C(98.6°F), and hypothermia sets in when the core body temperature gets lower than 35 °C (95 °F). Usually caused by prolonged exposure to cold temperatures, hypothermia is usually treated by methods that attempt to raise the body temperature back to a normal range. It was not until the introduction of thermometers that any exact data on the temperature of animals could be obtained. It was then found that local differences were present, since heat production and heat loss vary considerably in different parts of the body, although the circulation of the blood tends to bring about a mean temperature of the internal parts. Hence it is important to identify the parts of the body that most closely reflect the temperature of the internal organs. Also, for such results to be comparable, the measurements must be conducted under comparable conditions. The rectum has traditionally been considered to reflect most accurately the temperature of internal parts, or in some cases of sex or species, the vagina, uterus or bladder.

Thermogenesis is the process of heat production in organisms. It occurs in all warm-blooded animals, and also in a few species of thermogenic plants such as the Eastern skunk cabbage, the Voodoo lily, and the giant water lilies of the genus Victoria. The lodgepole pine dwarf mistletoe, Arceuthobium americanum, disperses its seeds explosively through thermogenesis.

<span class="mw-page-title-main">Fat-tailed dwarf lemur</span> Species of lemur

The fat-tailed dwarf lemur, also known as the lesser dwarf lemur, western fat-tailed dwarf lemur, or spiny forest dwarf lemur, is endemic to Madagascar.

<span class="mw-page-title-main">Heterothermy</span> Metabolic system

Heterothermy or heterothermia is a physiological term for animals that vary between self-regulating their body temperature, and allowing the surrounding environment to affect it. In other words, they exhibit characteristics of both poikilothermy and homeothermy.

<i>Antechinus</i> Genus of marsupials

Antechinus is a genus of small dasyurid marsupial endemic to Australia. They resemble mice with the bristly fur of shrews.

<span class="mw-page-title-main">Diurnality</span> Behavior characterized by activity during the day and sleeping during the night

Diurnality is a form of plant and animal behavior characterized by activity during daytime, with a period of sleeping or other inactivity at night. The common adjective used for daytime activity is "diurnal". The timing of activity by an animal depends on a variety of environmental factors such as the temperature, the ability to gather food by sight, the risk of predation, and the time of year. Diurnality is a cycle of activity within a 24-hour period; cyclic activities called circadian rhythms are endogenous cycles not dependent on external cues or environmental factors except for a zeitgeber. Animals active during twilight are crepuscular, those active during the night are nocturnal and animals active at sporadic times during both night and day are cathemeral.

<span class="mw-page-title-main">Kultarr</span> Species of marsupial

The kultarr is a small insectivorous nocturnal marsupial inhabiting the arid interior of Australia. Preferred habitat includes stony deserts, shrubland, woodland, grassland and open plains. The kultarr has a range of adaptations to help cope with Australia's harsh arid environment including torpor similar to hibernation that helps conserve energy. The species has declined across its former range since European settlement due to changes in land management practices and introduced predators.

<span class="mw-page-title-main">Fat-tailed dunnart</span> Species of mammal

The fat-tailed dunnart is a species of mouse-like marsupial of the Dasyuridae, the family that includes the little red kaluta, quolls, and the Tasmanian devil.

<span class="mw-page-title-main">Stripe-faced dunnart</span> Species of marsupial

The striped-faced dunnart is a small, Australian, nocturnal, "marsupial mouse," part of the family Dasyuridae. The species' distribution occurs throughout much of inland central and northern Australia, occupying a range of arid and semi-arid habitats.

<span class="mw-page-title-main">Little broad-nosed bat</span> Species of bat

The little broad-nosed bat translates to "Grey’s darkness creeper". Sometimes called Grey’s broad-nosed after the third governor of South Australia, Sir John Edward Grey. It is a species of vesper bat, which is one of the largest and best-known family of bats. They are endemic to Australia, are insectivores and have a broad range within the mainland, mainly in hot arid areas but also found in tropical rainforests.

<i>Histiotus</i> Genus of bats

Histiotus is a genus of South American vesper bats with species that include:

In chronobiology, the circannual cycle is characterized by biological processes and behaviors recurring on an approximate annual basis, spanning a period of about one year. This term is particularly relevant in the analysis of seasonal environmental changes and their influence on the physiology, behavior, and life cycles of organisms. Adaptations observed in response to these circannual rhythms include fur color transformation, molting, migration, breeding, fattening and hibernation, all of which are inherently driven and synchronized with external environmental changes.

Ozimops petersi, the inland free-tailed bat is a species of bat found in Australia.

Nicholas Mrosovsky was a Canadian zoologist known for his research in the fields of homeostasis, chronobiology, and sea turtle biology. He spent his whole professional career at the University of Toronto. His laboratory was notable for its seminal investigations of the influence of behavioural arousal on circadian rhythms. He was also the founder, in 1976, of Marine Turtle Newsletter. He received a Guggenheim Fellowship in 1973, and in 1993 he was elected a Fellow of the Royal Society of Canada.