Skip to main content
SpringerLink
Log in

Metabolic Depression: A Historical Perspective

  • Chapter
  • First Online:
Aestivation

Part of the book series: Progress in Molecular and Subcellular Biology ((PMSB,volume 49))

Abstract

An extended period of inactivity and reduced metabolic rate of many animals and plants, as well as unicellular organisms, has long been recognized by natural historians, e.g., Aristotle and Pliny. Biologists have studied this phenomenon since the 1550s (Gessner) and 1700s (Van Leeuwenhoek, Buffon). The period of inactivity can be less than a day, a few consecutive days or weeks, an entire season, or even many years. It can involve very different physiological states in response to a variety of environmental stimuli, such as extreme temperatures or unavailability of food or water. These periods of inactivity have been described and classified according to the group of organisms in question, extent and duration of the metabolic depression, ambient and body temperatures, state of body water (frozen or hyperosmotic), or availability of oxygen. Cryptobiosis, or “hidden life,” is an extreme form of inactivity, with often complete cessation of metabolism. It was first described in the 1700s, was further characterized in the 1800s, and in the 1900s physiological studies delineated the extent of metabolic depression. Molecular mechanisms for cryptobiosis have been sought since the late 1900s. Cryptobiosis includes three physiological states, anhydrobiosis (desiccation), osmobiosis (high osmotic concentration), and cryobiosis (freezing), where metabolic depression is associated with an altered physical state of cell water and often involves accumulation of compatible solutes, and one physiological state, anoxybiosis (anoxia), where metabolic depression occurs at the normal cellular hydration state. Dormancy (torpor) is a less extreme form of inactivity, associated with a moderate reduction in metabolic rate (hypometabolism). Although first described by Aristotle and Pliny, studies in the 1900s delineated the basic physiological changes that accompany dormancy. Dormancy allows avoidance of unfavorable short- or long-term climatic conditions and conservation of energy and water. Hibernation is long-term multiday torpor during winter, whereas aestivation is dormancy during summer. In ectotherms, the metabolic depression that accompanies dormancy is intrinsic, with metabolic rate declining to about 10 to 20% of resting metabolic rate at the same body temperature. The molecular mechanisms for intrinsic metabolic depression are poorly understood. In endotherms, torpor involves a fundamental physiological change in body temperature regulation that markedly reduces metabolic rate and water loss, often to <10% of the normothermic resting metabolic rate at the same ambient temperature. Most of this reduction in metabolic rate reflects the decreased setpoint for thermoregulation resulting in reduced metabolic heat production and a Q10 effect; there may be some intrinsic molecular-based metabolic depression in some hibernators. Dormancy allows species to exploit ephemeral environments and colonise habitats that would otherwise be unsuitable for growth or survival at certain times of the year. There are costs to dormancy, but for many species, the energetic and hygric advantages outweigh these costs.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aarset AV (1982) Freezing tolerance in intertidal invertebrates (a review). Comp Biochem Physiol A 73:571–580

    Google Scholar 

  • Abe AS (1995) Aestivation in South American amphibians and reptiles. Braz J Med Biol Res 28:1241–1247

    CAS  PubMed  Google Scholar 

  • Abe AS, Buck N (1985) Oxygen uptake of active and aestivating earthworm Glossoscolex paulistus (Oligochaeta, Glossoscolecidae). Comp Biochem Physiol A 81:63–66

    Google Scholar 

  • Anonymous (2003) Glossary of terms for thermal physiology. J Therm Biol 28:75–106

    Google Scholar 

  • Baker FC (1934) A conchological Rip Van Winkle. Nautilus 48:5–6

    Google Scholar 

  • Baker H (1753) Employment for the Microscope. Dodsley, London

    Google Scholar 

  • Barclay RMR, Lausen CL, Hollis L (2001) What’s hot and what’s not: defining torpor in free-ranging birds and mammals. Can J Zool 79:1885–1890

    Google Scholar 

  • Becquerel P (1907) Recherché sur la vie latent des grains. Ann Sci Nat (9e s. Bot) 5:193–311

    Google Scholar 

  • Buffenstein R (1985) The effect of starvation, food restriction and water deprivation on thermoregulation and average daily metabolic rates in Gerbillus pusillus. Physiol Zool 58:320–328

    Google Scholar 

  • Carpenter RE (1969) Structure and function of the kidney and the water balance of desert bats. Physiol Zool 42:288–302

    Google Scholar 

  • Christian KA, Corbett LK, Green B (1995) Seasonal activity and energetics of two species of varanid lizards in tropical Australia. Oecologia 103:349–357

    Google Scholar 

  • Christian KA, Green B, Kennett R (1996) Some physiological consequences of aestivation by freshwater crocodiles, Crocodylus johnstoni. J Herpetol 30:1–9

    Google Scholar 

  • Churchill TA, Storey KB (1996) Organ metabolism and cryoprotectant synthesis during freezing in spring peepers Pseudacris crucifer. Copeia 1996:517–525

    Google Scholar 

  • Claussen DL, Townsley MD, Bausch RG (1990) Supercooling and freeze tolerance in the European wall lizard, Podarcis muralis. J Comp Physiol B 160:137–143

    Google Scholar 

  • Clegg JS (1975) Metabolic consequences and the extent and disposition of the aqueous intracellular environment. J Exp Zool 215:303–313

    Google Scholar 

  • Clegg JS (1976) Interrelationships between water and metabolism in Artemia cysts–III. Respiration. Comp Biochem Physiol A 53:89–93

    CAS  PubMed  Google Scholar 

  • Clegg JS (1997) Embryos of Artemia franciscana survive four years of continuous anoxia: the case for complete metabolic rate depression. J Exp Biol 200:467–475

    PubMed  Google Scholar 

  • Clegg JS (2001) Cryptobiosis – a peculiar state of biological organization. Comp Biochem Physiol B 128:613–624

    CAS  PubMed  Google Scholar 

  • Clegg JS, Drinkwater LE, Sorgloos P (1996) The metabolic status of diapauses embryos of Artemia franciscana. Physiol Zool 69:49–66

    Google Scholar 

  • Coles GC (1968) The termination of aestivation in the large freshwater snail Pila ovate (Ampularidae) – I. Changes in oxygen uptake. Comp Biochem Physiol 25:517–522

    CAS  PubMed  Google Scholar 

  • Cooper CE, Geiser F (2008) The “minimum boundary curve for endothermy” as a predictor of heterothermy in mammals and birds: a review. J Comp Physiol B 178:1–8

    PubMed  Google Scholar 

  • Cooper CE, Geiser F, McAllan B (2005) Effect of torpor on the water economy of an arid-zone dasyurid, the stripe-faced dunnart (Sminthopsis macroura). J Comp Physiol B 175:323–328

    CAS  PubMed  Google Scholar 

  • Cooper CE, Kortner G, Brigham M, Geiser F (2008) Body temperature and activity patterns of free-living laughing kookaburras: the largest kingfisher is herterothermic. Condor 110:110–115

    Google Scholar 

  • Cooper CE, Withers PC, Cruz-Neto AP (2009) Metabolic, ventilatory and hygric physiology of the gracile mouse opossum (Gracilinanus agilis). Physiol Biochem Zool 82:153–162

    CAS  PubMed  Google Scholar 

  • Costanzo JP, Grenot C, Lee RE (1995) Supercooling, ice inoculation and freeze tolerance in the European common lizard, Lacerta vivipara. J Comp Physiol B 165:238–244

    Google Scholar 

  • Costanzo JP, Claussen DL, Lee RE (1988) Natural freeze tolerance in a reptile. Cryo Letters 9:380–385

    Google Scholar 

  • Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Hibernation in a tropical primate. Nature 429:825–826

    CAS  PubMed  Google Scholar 

  • Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2005) Hibernation in the tropics: lessons from a primate. J Comp Physiol B 175:147–155

    PubMed  Google Scholar 

  • Davis DE (1976) Hibernation and circannual rhythms of food consumption in marmots and ground squirrels. Q Rev Biol 54:477–514

    Google Scholar 

  • Davis WH (1970) Hibernation: ecology and physiological ecology. In: Wimsatt WA (ed) Biology of Bats, vol 1. Academic, New York, pp 266–300

    Google Scholar 

  • Delaney RG, Lahiri S, Fishman AP (1974) Aestivation in the African lungfish Protopterus aethiopicus: cardiovascular and respiratory functions. J Exp Biol 61:111–128

    CAS  PubMed  Google Scholar 

  • Dinkelacker SA, Costanzo JP, Lee RE (2005) Anoxia tolerance and freeze tolerance in hatchling turtles. J Comp Physiol B 175:209–217

    CAS  PubMed  Google Scholar 

  • Donohoe PH, Boutilier RG (1998) The protective effects of metabolic rate depression in hypoxic cold submerged frogs. Respir Physiol 111:325–336

    CAS  PubMed  Google Scholar 

  • Donohoe PH, West TG, Boutilier RG (1998) Respiratory, metabolic, and acid-base correlates of aerobic metabolic rate reduction in overwintering frogs. Am J Physiol 274:R704–R710

    CAS  PubMed  Google Scholar 

  • Duman JG, Wu DW, Xu L, Tursman D, Olsen TM (1991) Adaptations of insects to subzero temperatures. Q Rev Biol 66:387–410

    Google Scholar 

  • Eisentraut M (1934) Der winterschlaf der fledermäuse mit besonderer berücksichtigung der wärme-regulation. Z Morph Ökol 29:231–267

    Google Scholar 

  • Etheridge K (1990) The energetics of aestivating sirenid salamanders (Siren lacertina and Pseudobranchus striatus). Herpetologica 46:407–414

    Google Scholar 

  • Ewart AJ (1908) On the longevity of seeds. Proc Roy Soc Vict 21:1–210

    Google Scholar 

  • Florant GL, Heller HC (1977) CNS regulation of body temperature in euthermic and hibernating marmots (Marmota flaviventris). Am J Physiol 232:R203–R208

    CAS  PubMed  Google Scholar 

  • Gavaret J (1859) Quelques experiences sur les rotifers, les tardigrades et les anguillules des mousses des toits. Ann Sci Nat Zool 11:315–330

    Google Scholar 

  • Geiser F, Coburn DK, Körtner G, Law BS (1996) Thermoregulation, energy metabolism, and torpor in blossom-bats Synconycteris australis (Megachiroptera). J Zool 239:583–590

    Google Scholar 

  • Geiser F (1988) Reduction of metabolism during hibernation and daily torpor in mammals and birds: temperature effect or physiological inhibition? J Comp Physiol B 158:25–37

    CAS  PubMed  Google Scholar 

  • Geiser F (1994) Hibernation and daily torpor in marsupials: a review. Aust J Zool 42:1–16

    Google Scholar 

  • Geiser F (2004a) Metabolic rate and body temperature reduction during hibernation and daily torpor. Ann Rev Physiol 66:239–274

    CAS  Google Scholar 

  • Geiser F (2004b) The role of torpor in the life of Australian arid zone mammals. Aust Mammal 26:125–134

    Google Scholar 

  • Geiser F, Ruf T (1995) Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol Zool 68:935–966

    Google Scholar 

  • Geiser F, Goodship N, Pavey CR (2002) Was basking important in the evolution of mammalian endothermy? Naturwissenschaften 89:412–414

    CAS  PubMed  Google Scholar 

  • Glasheen JS, Hand SC (1989) Metabolic heat dissipation and internal solute levels of Artemia embryos during changes in cell-associated water. J Exp Biol 145:263–282

    Google Scholar 

  • Glazer I, Salame L (2000) Osmotic survival of the entomopathogenic nematode Steinernema carpocapsae. Biol Control 18:251–257

    Google Scholar 

  • Gregory PT (1982) Reptilian hibernation. In: Gans C, Pough FH (eds) Biology of the Reptilia. Academic Press, London, pp 53–154

    Google Scholar 

  • Guppy MG, Withers PC (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev 7:1–40

    Google Scholar 

  • Hailey A, Loveridge JP (1997) Metabolic depression during dormancy in the African tortoise Kinixys spekii. Can J Zool 75:1328–1335

    Google Scholar 

  • Hartner WC, South FE, Jacobs HK, Luecke RH (1971) Preoptic thermal stimulation and temperature regulation in the marmot (M. flaviventris). Cryobiology 8:312–313

    Google Scholar 

  • Heller HC, Colliver GW (1974) CNS regulation of body temperature during hibernation. Am J Physiol 227:583–589

    CAS  PubMed  Google Scholar 

  • Heller HC, Walker JM, Florant GL, Glotzbach SF, Berger RJ (1978) Sleep and hibernation: electrophysiological and thermoregulatory homologies. In: Wang LC, Hudson JW (eds) Strategies in the Cold: Natural Torpidity and Thermogenesis. Academic, London, pp 225–265

    Google Scholar 

  • Hillman SS, Withers PC, Drewes RC, Hillyard S (2008) Ecological and environmental physiology of amphibians. Oxford University Press, Oxford

    Google Scholar 

  • Hochachka PW, Lutz PL (2001) Mechanism, origin, and evolution of anoxia tolerance in animals. Comp Biochem Physiol B 130:435–459

    CAS  PubMed  Google Scholar 

  • Hudson JW (1978) Shallow daily torpor: a thermoregulatory adaptation. In: Wang LC, Hudson JW (eds) Strategies in the Cold: Natural Torpidity and Thermogenesis. Academic, London, pp 67–108

    Google Scholar 

  • Jackson DC (1968) Metabolic depression and oxygen depletion in the diving turtle. J Appl Physiol 24:503–509

    CAS  PubMed  Google Scholar 

  • Jackson DC (2000) Living without oxygen: lessons from the freshwater turtle. Comp Biochem Physiol A 125:299–315

    CAS  Google Scholar 

  • Jaeger EC (1948) Does the poor-will “hibernate”? Condor 50:45–46

    Google Scholar 

  • Jaeger EC (1949) Further observations on the hibernation of the poor-will. Condor 51:105–109

    Google Scholar 

  • Kayser C (1961) The Physiology of Natural Hibernation. Pergamon, London

    Google Scholar 

  • Keilin D (1959) The problem of anabiosis or latent life: history and current concept. Proc Roy Soc Lond 150:149–191

    CAS  Google Scholar 

  • Keister M, Buck J (1964) Respiration: some exogenous and endogenous effects on rate of respiration. In: Rockstein R (ed) The physiology of the Insecta, vol III. Academic Press, New York, pp 617–658

    Google Scholar 

  • Kennett R, Christian K (1994) Metabolic depression in estivating long-neck turtles (Chelodina rugosa). Physiol Zool 67:1087–1102

    Google Scholar 

  • Lasiewski RC (1964) Body temperatures, heart and breathing rate and evaporative water loss in humming birds. Physiol Zool 37:212–223

    Google Scholar 

  • Laverack MS (1963) The Physiology of Earthworms. Pergamon, Oxford

    Google Scholar 

  • Lee AK, Mercer EH (1967) Cocoon surrounding desert-dwelling frogs. Science 157:87–88

    CAS  PubMed  Google Scholar 

  • Lees AD (1955) The Physiology of Diapause in Arthropods. Cambridge University Press, Cambridge

    Google Scholar 

  • Lees AD (1956) The physiology and biochemistry of diapauses. Ann Rev Entomol 1:1–16

    CAS  Google Scholar 

  • Loomis SH (1987) Freezing in intertidal invertebrates. Cryo Letters 8:186–195

    Google Scholar 

  • Lyman CP (1948) The oxygen consumption and temperature regulation of hibernating hamsters. J Exp Zool 109:55–78

    CAS  PubMed  Google Scholar 

  • Lyman CP (1970) Thermoregulation and metabolism in bats. In: Wimsatt WA (ed) Biology of Bats, vol 1. Academic, New York, pp 301–330

    Google Scholar 

  • Lyman CP (1978) Natural torpidity, problems and perspectives. In: Wang LC, Hudson JW (eds) Strategies in the Cold: Natural Torpidity and Thermogenesis. Academic, London, pp 9–19

    Google Scholar 

  • Lyman CP, Willis JS, Malan A, Wang LC (1982) Hibernation and Torpor in Mammals and Birds. Academic, New York

    Google Scholar 

  • MacMillen RE (1965) Aestivation in the cactus mouse Peromyscus eremicus. Comp Biochem Physiol 16:227–248

    CAS  PubMed  Google Scholar 

  • MacMillen RE, Greenaway P (1978) Adjustments of energy and water metabolism to drought in an Australian arid-zone crab. Physiol Zool 51:239–240

    Google Scholar 

  • Mayhew WW (1965) Hibernation in the horned lizard, Phrynosoma m’calli. Comp Biochem Physiol 16:103–119

    CAS  PubMed  Google Scholar 

  • McAtee WL (1947) Torpidity in birds. Am Midl Nat 38:191–206

    Google Scholar 

  • McClanahan LL (1967) Adaptations of the spadefoot toad, Scaphiopus couchi, to desert environments. Comp Biochem Physiol 20:73–99

    CAS  Google Scholar 

  • McClanahan LL, Ruibal R, Shoemaker VH (1983) Rate of cocoon formation and physiological its correlates in a ceratophryid frog. Physiol Zool 56:430–435

    Google Scholar 

  • McKechnie AE, Lovegrove BG (2002) Avian facultative hypothermic responses: a review. Condor 104:705–724

    Google Scholar 

  • Mills SC, South FE (1972) Central regulation of temperatue in hibernation and normothermia. Cryobiology 9:393–403

    CAS  PubMed  Google Scholar 

  • Moberley WR (1963) Hibernation in the desert iguana, Dipsosaurus dorsalis. Physiol Zool 36:152–160

    Google Scholar 

  • Mrosovsky N (1971) Hibernation and Hypothalamus. Appleton-Century-Crofts, New York

    Google Scholar 

  • Mrosovsky N (1990) Rheostasis. The Physiology of Change. Oxford University Press, New York

    Google Scholar 

  • Nagy KA, Medica PA (1986) Physiological ecology of desert tortoises in southern Nevada. Herpetologica 42:73–92

    Google Scholar 

  • Nagy KA, Shoemaker VH (1975) Energy and nitrogen budgets of the free-living desert lizard Sauromalus obesus. Physiol Zool 48:252–262

    Google Scholar 

  • Needham JT (1743) A letter concerning chalky tubulous concretions, with some microscopical observations on the farina of the red lily, and on worms discovered in smutty corn. Phil Trans R Soc Lond 42:634–641

    Google Scholar 

  • Nelson DR (2002) Current status of the Tardigrada: evolution and ecology. Integr Comp Biol 42:652–659

    Google Scholar 

  • Ohga I (1923) On the longevity of the fruits of Nelumbo nucifera. Bot Mag Tokyo 37:87

    Google Scholar 

  • Pearson OP (1960) Torpidity in birds. In: Lyman CP, Dawe AR (eds) Mammalian Hibernation. Bull Mus Comp Zool 124:93–103

    Google Scholar 

  • Pedler S, Fuery CJ, Withers PC, Flanigan J, Guppy M (1996) Effectors of metabolic depression in an estivating pulmonate snail (Helix aspersa): whole animal and in vitro tissue studies. J Comp Physiol 166:375–381

    CAS  Google Scholar 

  • Podrabsky JE, Hand SC (1999) The bioenergetics of embryonic diapause in an annual killifish, Austrofundulus limnaeus. J Exp Biol 202:2567–2580

    CAS  PubMed  Google Scholar 

  • Podrabsky JE, Carpenter JF, Hand SC (2001) Survival of water stress in annual killifish embryos: dehydration avoidance and egg envelope amyloid fibers. Am J Physiol Int Comp Physiol 280:R123–R131

    CAS  Google Scholar 

  • Preyer W (1891) Uber de anabiose. Biol Zbl 11:1–5

    Google Scholar 

  • Pusey BJ (1990) Seasonality, aestivation and the life history of the salamander fish Lepidogalaxias salamandroides (Pisces: Lepidogalaxiidae). Environ Biol Fishes 29:15–26

    Google Scholar 

  • Rakshpal R (1962) Respiratory metabolism during embryogenesis of a diapauses species of field cricket, Gryllus pennsylvanicus Burmeister (Orthoptera: Gryllidae). J Insect Physiol 8:217–221

    CAS  Google Scholar 

  • Rasmussen AT (1916) Theories of hibernation. Am Nat 50:609–625

    Google Scholar 

  • Réaumur RA (1737) Des chenilles qui vivent en société. In: Mortier P (ed) Mémoires pour servir á l’Histoire des Insectes, vol 2. Pierre Mortier, Amsterdam, pp 153–225

    Google Scholar 

  • Rebecchi L, Altiero T, Guidetti R (2007) Anhydrobiosis: the extreme limit of desiccation tolerance. Invert Surv J 4:65–81

    Google Scholar 

  • Reeder WG (1949) Hibernating temperature of the bat, Myotis californicus pallidus. J Mamm 30:51–53

    CAS  Google Scholar 

  • Righi G (1972) Bionomic considerations upon the Glossoscoleidae (Oligochaeta). Pedobiologia 12:254–260

    Google Scholar 

  • Ring RA (1981) The physiology and biochemistry of cold tolerance in Arctic insects. J Therm Biol 6:219–229

    CAS  Google Scholar 

  • Ruschi A (1949) Observations on the Trochilidae. Bull Mus Biol Prof Mello-Leitão, vol 7. Santa Teresa, Brazil

    Google Scholar 

  • Schmid WD (1982) Survival of frogs in low temperature. Science 215:697–698

    CAS  PubMed  Google Scholar 

  • Schmidt P (1948) Anabiosis. USSR Acadamey of Science, Moscow and Leningrad

    Google Scholar 

  • Seidel ME (1978) Terrestrial dormancy in the turtle Kinosternum flavescens: respiratory metabolism and dehydration. Comp Biochem Physiol A 61:1–4

    Google Scholar 

  • Seymour RS (1973) Energy metabolism of dormant spadefoot toads (Scaphiopus). Copeia 1973:435–445

    Google Scholar 

  • Smith HW (1930) Metabolism of the lungfish Protopterus aethiopicus. J Biol Chem 88:97–130

    CAS  Google Scholar 

  • South FE, Breazile JE, Dellman HD, Epperly AD (1969) Sleep, hibernation and hypothermia in the yellow-bellied marmot (M. flaviventris). In: Mussacchia XJ, Saunders JF (eds) Depressed Metabolism. New York, Elsevier, pp 277–312

    Google Scholar 

  • Spallanzani L (1776) Opuscoli di fisica animale e vegetabile. Societa Tipografica (Modena) 2:203–285

    Google Scholar 

  • Spencer B (1896) Report on the work of the Horn scientific expedition to Central Australia. Part II. Zoology. Dulau, London

    Google Scholar 

  • Steiner G, Albin FE (1946) Rescusitation of the nematode Tylenchis polyhypnus sp., after almost 39 years’ dormancy. J Wash Acad Sci 36:97–99

    CAS  PubMed  Google Scholar 

  • Storey KB (1996) Metabolic adaptations supporting anoxia tolerance in reptiles: recent advances. Comp Biochem Physiol B 113:23–35

    CAS  PubMed  Google Scholar 

  • Storey KB (2001) Molecular Mechanisms of Metabolic Arrest. Life in Limbo. Bios Scientific, Oxford

    Google Scholar 

  • Storey KB, Storey JM (1986) Freeze tolerant frogs: cryoprotectants and tissue metabolism during freeze/thaw cycles. Can J Zool 64:49–56

    CAS  Google Scholar 

  • Storey KB, Storey JM (1988) Freeze tolerance in animals. Physiol Rev 68:27–84

    CAS  PubMed  Google Scholar 

  • Storey KB, Storey JM (1989) Freeze tolerance and freeze-avoidance in ectotherms. In: Wang LCH (ed) Advances in Comparative and Environmental Physiology, vol 4. Springer, Berlin, pp 51–82

    Google Scholar 

  • Storey KB, Storey JM (1990) Facultative metabolic rate depression: molecular regulation and biochemical adaptation in anaerobiosis, hibernation and aestivation. Q Rev Biol 65:145–174

    CAS  PubMed  Google Scholar 

  • Storey KB, Storey JM (1991) Biochemistry of cryoprotectants. In: Denlinger DL, Lees RE (eds) Insects at Low Temperatures. Chapman, New York, pp 64–93

    Google Scholar 

  • Storey KB, Storey JM (1996) Natural freezing survival in animals. Annu Rev Ecol Syst 27:365–386

    Google Scholar 

  • Storey KB, Storey JM, Brooks SP, Churchill TA, Brooks RJ (1988) Hatchling turtles survive freezing during winter hibernation. Proc Natl Acad Sci USA 85:8350–8354

    CAS  PubMed  Google Scholar 

  • Taplin LE (1988) Osmoregulation in crocodilians. Biol Rev 63:333–377

    Google Scholar 

  • Thomas DW, Geiser F (1997) Periodic arousals in hibernating mammals: is evaporative water loss involved? Funct Ecol 11:585–591

    Google Scholar 

  • Tunnacliffe A, Lapinski J (2003) Resurrecting van Leeuwenhoek’s rotifers: a reappraisal of the role of disaccharides in anhydrobiosis. Philos Trans R Soc London B 358:1755–1771

    CAS  Google Scholar 

  • Turner JH (1933) The viability of seeds. Kew Bull 6:251

    Google Scholar 

  • Van Beurden E (1980) Energy metabolism of dormant Australian water-holding frogs (Cyclorana platycephala). Copeia 1980:787–799

    Google Scholar 

  • Van Gundy SD (1965) Factors in survival of nematodes. Annu Rev Phytopathol 3:43–68

    Google Scholar 

  • Van Leeuwenhoek A (1702) On certain animalcules found in the sediments in gutter of the roofs of houses. Letter 144, to Hendrik van Bleyswijk. In: Selected Works of Anton van Leeuwenhoek, vol 2. London. pp. 207–213

    Google Scholar 

  • Watanabe M (2006) Anhydrobiosis in invertebrates. Appl Entomol Zool 41:15–31

    CAS  Google Scholar 

  • Weigmann R (1929) Die Wirkung starker Abkfihlung auf Amphibien und Reptitien. Z Wiss Zool 134:641–692

    CAS  Google Scholar 

  • Wharton DA (2002) Life at the limits. Organisms in extreme environments. Cambridge University Press, Cambridge

    Google Scholar 

  • Withers PC (1992) Comparative animal physiology. Saunders College Publishing, Philadelphia

    Google Scholar 

  • Withers PC (1993) Metabolic depression during aestivation in the Australian frogs, Neobatrachus and Cyclorana. Aust J Zool 41:467–473

    Google Scholar 

  • Womersley C (1981) Biochemical and physiological aspects of anhydrobiosis. Comp Biochem Physiol B 70:668–678

    Google Scholar 

  • Wright JC (2001) Cryptobiosis 300 years on from van Leuwenhoek: what have we learned about tardigrades? Zool Anz 240:563–582

    Google Scholar 

  • Wright JC, Westh P, Ramløv H (1992) Cryptobiosis in Tardigrada. Biol Rev 67:1–29

    Google Scholar 

  • Zachariassen KE (1985) Physiology of cold tolerance in insects. Physiol Rev 65:799–832

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Carlos Navas and José Eduardo de Carvalho for their invitation to contribute to this book, Ariovaldo P. Cruz Neto for valuable discussion, and the reviewer for useful comments on the draft manuscript

Author information

Authors and Affiliations

  1. Department of Zoology, School of Animal Biology M092, University of Western Australia, Crawley, 6009, Western Australia, Australia

    Philip C. Withers & Christine E. Cooper

  2. Department of Environmental and Aquatic Science, Curtin University of Technology, U1987, Perth, 6845, Western Australia, Australia

    Philip C. Withers & Christine E. Cooper

Authors
  1. Philip C. Withers
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christine E. Cooper
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Philip C. Withers .

Editor information

Editors and Affiliations

  1. Instituto de Biociências, Universidade de São Paulo, Rua do Matao 14, São Paulo, 05508-900, Brazil

    Carlos Arturo Navas

  2. Universidade Federal de São Paulo, Rua Prof. Artur Riedel 275, Diadema, 09972-270, Brazil

    José Eduardo Carvalho

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Withers, P.C., Cooper, C.E. (2010). Metabolic Depression: A Historical Perspective. In: Arturo Navas, C., Carvalho, J. (eds) Aestivation. Progress in Molecular and Subcellular Biology, vol 49. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-02421-4_1

Download citation

Publish with us

Policies and ethics

Search

Navigation