Abstract
The ability to reduce metabolic rate during exposure to environmental stress, termed metabolic rate suppression, is thought to be an important component to enhance survival in many organisms. Metabolic rate suppression can be achieved through modifications to behavior, physiology, and cellular biochemistry, all of which act to reduce whole organisms energy expenditure. This chapter will critically evaluate the use of metabolic rate suppression as a response to environmental challenge in fish using three metabolic states: aestivation, hypoxia/anoxia exposure, and diapause.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Almeida-Val VM, Chippari-Gomes AR, Lopes NP (2006) Metabolic and physiological adjustments to low oxygen and high temperature in fishes of the amazon. In: Val AL, Almeida-Val VM, Randal DJ (eds) The physiology of tropical fishes, vol 21. Elsevier, San Diego, pp 443–491
Bickler PE, Buck LT (2007) Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annu Rev Physiol 69:145–170
Bogdanova A, Grenacher B, Nikinmaa M, Gassmann M (2005) Hypoxic responses of Na+/K+ ATPase in trout hepatocytes. J Exp Biol 208:1793–1801
Boutilier RG (2001) Mechanisms of cell survival in hypoxia and hypothermia. J Exp Biol 204:3171–3131
Boutilier RG, St-Pierre J (2000) Surviving hypoxia without really dying. Comp Biochem Physiol A 126:481–490
Buck LT, Hochachka PW (1993) Anoxic supression of Na+/K+-ATPase and constant membrance potenetial in hepatocytes: support for channel arrest. Am J Physiol 265:R1020–R1025
Buck LT, Hochachka PW, Schon A, Gnaiger E (1993a) Microcalorimetric measurement of reversible metabolic suppression induced by anoxia in isolated hepatocytes. Am J Physiol 265:R1014–R1019
Buck LT, Land SC, Hochachka PW (1993b) Anoxia-tolerant hepatocytes: model system for study of reversible metabolic suppression. Am J Physiol 265:R49–R56
Campbell HA, Fraser KPP, Bishop CM, Peck LS, Egginton S (2008) Hibernation in an Antarctic fish: on ice for winter. PLoS ONE 3:1–9
Carling D (2004) The AMP-activated protein kinase cascade – a unifying system for energy control. Trends Biochem Sci 29:18–24
Chapman LJ, McKenzie DJ (2009) Behavioural responses and ecological consequences. In: Richards JG, Farrell AP, Brauner CJ (eds) Hypoxia. Elsevier, San Diego
da Silva GDSF, Giusti H, Sanchez AP, do Carmo JM, Glass ML (2008) Aestivation in the South American lungfish, Lepidosiren paradoxa: effects on cardiovascular function, blood gases, osmolality and leptin levels. Respir Physiol Neurobiol 164:380–385
Darken RS, Martin KLM, Fisher MC (1998) Metabolism during delayed hatching in terrestrial eggs of a marine fish, the grunion Leuresthes tenuis. Physiol Zool 71:400–406
Delaney RG, Lahiri S, Fishman AP (1974) Estivation of African lungfish Protopterus aethiopicus: Cardiovascular and respiratory functions. J Exp Biol 61:111–128
Diaz RJ, Breitburg DL (2009) The hypoxic environment. In: Richards JG, Farrell AP, Brauner CJ (eds) Hypoxia. Elsevier, San Diego
Eduardo J, Bicudo PW, Johansen K (1979) Respiratory gas exchange in the airbreathing fish, Synbranshus marmoratus. Environ Biol Fish 4:55–64
Fergusson-Kolmes L, Podrabsky JE (2007) Differential effects of anoxia on heart rate in developmental stages of the annual killifish Austrofundulus limnaeus that differ in their tolerance of anoxia. J Exp Zool A 307:419–423
Fishman AP, Galante RJ, Winokur A, Pack AI (1992) Estivation in the African lungfish. Proc Am Philos Soc 136:61–72
Fishman AP, Pack AI, Delaney RG, Galante RJ (1986) Estivation in Protopterus. J Morphol 1(Suppl):237–248
Fitzgibbon QP, Seymour RS, Ellis D, Buchanan J (2007) The energetic consequence of specific dynamic action in southern bluefin tuna Thunnus maccoyii. J Exp Biol 210:290–298
Frick NT, Bystriansky JS, Ip YK, Chew SF, Ballantyne JS (2008a) Carbohydrate and amino acid metabolism in fasting and aestivating African lungfish (Protopterus dolloi). Comp Biochem Physiol A 151:85–92
Frick NT, Bystriansky JS, Ip YK, Chew SF, Ballantyne JS (2008b) Lipid, ketone body and oxidative metabolism in the African lungfish, Protopterus dolloi following 60 days of fasting and aestivation. Comp Biochem Physiol A 151:93–101
Fry FEJ (1971) The effect of environmental factors on the physiology of fish. In: Hoar WS, Randal DJ (eds) Fish physiology: environmental relations and behaviour, vol VI. Academic, New York, pp 1–98
Gamperl K, Driedzic WR (2009) Cardiovascular funciton and cardiac metabolism during environmental hypoxia. In: Richards JG, Farrell AP, Brauner CJ (eds) Hypoxia. Elsevier, San Diego
Graham JB (1997) Air-breathing fishes: evolution, diversity and adapatation. Academic, San Diego
Greenwood PH (1986) The natural history of African lungfishes. J Morphol 1:163–179
Guppy M (2004) The biochemistry of metabolic depression: a history of perceptions. Comp Biochem Physiol B 139:435–442
Hand SC, Hardewig I (1996) Downregulation of cellular metabolism during environmental stress: mechanisms and implications. Annu Rev Physiol 58:539–563
Hardie DG, Pan DA (2002) Regulation of fatty acid synthesis and oxidation by the AMP-activated protein kinase. Biochem Soc Trans 30:1064–1070
Hochachka P, Somero GN (2002) Biochemical Adaptation: mechanism and process in physiological evolution. Oxford University Press, New York
Hochachka PW, Buck LT, Doll CJ, Land SC (1996) Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci USA 93:9493–9498
Hochachka PW, Guppy M (1987) Metabolic arrest and the control of biological time. Harvard University Press, Cambridge, MA
Hochachka PW, Lutz PL (2001) Mechanism, origin, and evolution of anoxia tolerance in animals. Comp Biochem Physiol B 130:435–459
Holmes BF, Kurth-Kraczek EJ, Winder WW (1999) Chronic activation of 5′-AMP-activated protein kinase increases GLUT-4, hexokinase, and glycogen in muscle. J Appl Physiol 87:1990–1995
Horman S, Browne G, Krause U, Patel J, Vertommen D, Bertrand L, Lavoinne A, Hue L, Proud C, Rider M (2002) Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis. Curr Biol 12:1419–1423
Hylland P, Milton S, Pek M, Nilsson GE, Lutz PL (1997) Brain Na+/K+ATPase activity in two anoxia tolerant vertebrates: Crucian carp and freshwater turtle. Neurosci Lett 235:89–92
Jibb LA, Richards JG (2008) AMP-activated protein kinase activity during metabolic rate depression in the hypoxic goldfish, Carassius auratus. J Exp Biol 211:3111–3122
Johansson D, Nilsson G, Ouml TE (1995) Effects of anoxia on energy metabolism in crucian carp brain slices studied with microcalorimetry. J Exp Biol 198:853–859
Kind PK, Grigg GC, Booth DT (2002) Physiological responses to prolonged aquatic hypoxia in the Queensland lungfish Neoceratodus forsteri. Respir Physiol Neurobiol 132:179–190
Kurth-Kraczek EJ, Hirshman MF, Goodyear LJ, Winder WW (1999) 5′ AMP-activated protein kinase activation causes GLUT4 translocation in skeletal muscle. Diabetes 48:1667–1671
Land SC, Bernier NJ (1995) Estivation: mechanisms and control of metabolic suppression. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes, vol 5. Elsevier Science, New York, pp 381–412
Land SC, Buck LT, Hochachka PW (1993) Response of protein synthesis to anoxia and recovery in anoxia-tolerant hepatocytes. Am J Physiol 265:R41–R48
Lewis JM, Costa I, Val AL, Almeida-Val VM, Gamperl AK, Driedzic WR (2007) Responses to hypoxia and recovery: repayment of oxygen debt is not associated with compensatory protein synthesis in the Amazonian cichlid, Astronotus ocellatus. J Exp Biol 210:1935–1943
Lomholt JP (1993) Breathing in the aestivating African lungfish, Protopterus amphibious. Advan Fish Res 1:17–34
Loong AM, Ang SF, Wong WP, Portner HO, Bock C, Wittig R, Bridges CR, Chew SF, Ip YK (2008a) Effects of hypoxia on the energy status and nitrogen metabolism of African lungfish during aestivation in a mucus cocoon. J Comp Physiol B 178:853–865
Loong AM, Pang CYM, Hiong KC, Wong WP, Chew SF, Ip YK (2008b) Increased urea synthesis and/or suppressed ammonia production in the African lungfish, Protopterus annectens, during aestivation in air or mud. J Comp Physiol B 178:351–363
Machado BE, Podrabsky JE (2007) Salinity tolerance in diapausing embryos of the annual killifish Austrofundulus limnaeus is supported by exceptionally low water and ion permeability. J Comp Physiol B 177:809–820
Marsin AS, Bertrand L, Rider MH, Deprez J, Beauloye C, Vincent MF, Van den Berghe G, Carling D, Hue L (2000) Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr Biol 10:1247–1255
Matsumoto JK, Martin KLM (2008) Lethal and sublethal effects of altered sand salinity on embryos of beach-spawning California grunion. Copeia 2008:484–491
Mesquita-Saad LSB, Leitão MAB, Paula-Silva MN, Chippari-Gomes AR, Almeida-Val VM (2002) Specialized metabolism and biochemical suppression during aestivation of the extant south american lungfish – Lepidosiren paradoxa. Braz J Biol 62:495–501
Nielsen JN, Wojtaszewski JF, Haller RG, Hardie DG, Kemp BE, Richter EA, Vissing J (2002) Role of 5’AMP-activated protein kinase in glycogen synthase activity and glucose utilization: insights from patients with McArdle’s disease. J Physiol 541:979–989
Nikinmaa M, Rees BB (2005) Oxygen-dependent gene expression in fishes. Am J Physiol 288:R1079–R1090
Nilsson GE (1991) The adenosine receptor blocker aminophylline increases anoxic ethanol excretion in crucian carp. Am J Physiol 261:R1057–R1060
Nilsson GE (1992) Evidence for a role of GABA in metabolic depression during anoxia in crucian carp (Carassius carassius). J Exp Biol 165:243–259
Nilsson GE, Lutz PL (2004) Anoxia tolerant brains. J Cereb Blood Flow Metab 24:475–486
Nilsson GE, Rosen P, Johansson D (1993) Anoxic depression of spontaneous locomotor activity in crucian carp quantified by a computerized imaging technique. J Exp Biol 180:153–162
Perry SF, Euverman R, Wang T, Loong AM, Chew SE, Ip YK, Gilmour KM (2008) Control of breathing in African lungfish (Protopterus dolloi): A comparison of aquatic and cocooned (terrestrialized) animals. Respir Physiol Neurobiol 160:8–17
Perry SF, Gilmour KM, Swenson ER, Vulesevic B, Chew SF, Ip YK (2005) An investigation of the role of carbonic anhydrase in aquatic and aerial gas transfer in the African lungfish Protopterus dolloi. J Exp Biol 208:3805–3815
Perry SF, Jonz MG, Gilmour KM (2009) Oxygen sensing and the hypoxic ventilatory response. In: Richards JG, Farrell AP, Brauner CJ (eds) Hypoxia. Elsevier, San Diego
Podrabsky JE, Carpenter JF, Hand SC (2001) Survival of water stress in annual fish embryos: dehydration avoidance and egg envelope amyloid fibers. Am J Physiol 280:R123–R131
Podrabsky JE, Hand SC (1999) The bioenergetics of embryonic diapause in an annual killifish, Austrofundulus limnaeus. J Exp Biol 202:2567–2580
Podrabsky JE, Hand SC (2000) Depression of protein synthesis during diapause in embryos of the annual killifish Austrofundulus limnaeus. Physiol Biochem Zool 73:799–808
Podrabsky JE, Lopez JP, Fan TW, Higashi R, Somero GN (2007) Extreme anoxia tolerance in embryos of the annual killifish Austrofundulus limnaeus: insights from a metabolomics analysis. J Exp Biol 210:2253–2266
Pusey BJ (1990) Seasonality, estivation and the life history of the salamanderfish Lepidogalaxias salamandroides (Pisces, Lepidogalaxiidae). Env Biol Fish 29:15–26
Richards JG (2009) Metabolic and molecular responses of fish to hypoxia. In: Richards JG, Farrell AP, Brauner CJ (eds) hypoxia. Elsevier, San Diego
Richards JG, Wang YS, Brauner CJ, Gonzalez RJ, Patrick ML, Schulte PM, Choppari-Gomes AR, Almeida-Val VM, Val AL (2007) Metabolic and ionoregulatory responses of the Amazonian cichlid, Astronotus ocellatus, to severe hypoxia. J Comp Physiol B 177:361–374
Rissanen E, Tranberg HK, Nikinmaa M (2006) Oxygen availability regulates metabolism and gene expression in trout hepatocyte cultures. Am J Physiol 291:R1507–R1515
Smith HW (1930) Metabolism of the lungfish, Protopterus aethiopicus. J Biol Chem 88:97–130
Smith HW (1935) The metabolism of the lung fish. II. Effect of feeding meat on metabolic rate. J Cell Comp Physiol 6:335–349
Smith RW, Houlihan DF, Nilsson GE, Alexandre J (1999) Tissue-specific changes in RNA synthesis in vivo during anoxia in crucian carp. Am J Physiol 277:R690–R697
Smith RW, Houlihan DF, Nilsson GE, Brechin JG (1996) Tissue-specific changes in protein synthesis rates in vivo during anoxia in crucian carp. Am J Physiol 271:R897–R904
Stangl P, Wegener G (1996) Calorimetric and biochemical studies on the effects of environmental hypoxia and chemicals on freshwater fish. Thermochim Acta 271:101–113
Staples JF, Kajimura M, Wood CM, Patel M, Ip YK, McClelland GB (2008) Enzymatic and mitochondrial responses to 5 months of aerial exposure in the slender lungfish Protopterus dolloi. J Fish Biol 73:608–622
Steffensen JF, Lomholt JP (1983) Energetic cost of active branchial ventilation in the sharksucker, Echeneis naucrates. J Exp Biol 103:185–192
Stensløkken KO, Ellefsen S, Stecyk JAW, Dahl MB, Nilsson GE, Vaage J (2008) Differential regulation of AMP-activated kinase and AKT kinase in response to oxygen availability in crucian carp (Carassius carassius). Am J Physiol 295:R1803–R1814
Storey KB, Storey JM (2004) Metabolic rate depression in animals: transcriptional and translational controls. Biol Rev 79:207–233
van Ginneken VJ, van den Thillart GE, Muller HJ, van Deursen S, Onderwater M, Visee J, Hopmans V, van Vliet G, Nicolay K (1999) Phosphorylation state of red and white muscle in tilapia during graded hypoxia: an in vivo (31)P-NMR study. Am J Physiol 277:R1501–R1512
van Ginneken VJT, Addink ADF, van den Thillart GEEJM, Korner F, Noldus L, Buma M (1997) Metabolic rate and level of activity determined in tilapia (Oreochromis mossambicus Peters) by direct and indirect calorimetry and videomonitoring. Thermochim Acta 291:1–13
van Ginneken VJT, Onderwater M, Olivar OL, van den Thillart GEEJM (2001) Metabolic depression and investigation of glucose/ethanol conversion in the European eel (Anguilla anguilla Linnaeus 1758) during anaerobiosis. Thermochim Acta 373:23–30
van Ginneken VJT, Snelderwaard P, van der Linden R, van der Reijden N, van den Thillart GEEJM, Kramer K (2004) Coupling of heart rate with metabolic depression in fish: a radiotelemetric and calorimetric study. Thermochim Acta 414:1–10
van Waversveld J, Addink ADF, van den Thillart G (1989a) The anaerobic energy metabolism of goldfish determined by simultaneous direct and indirect calorimetry during anoxia and hypoxia. J Comp Physiol B 159:263–268
van Waversveld J, Addink ADF, van den Thillart G (1989b) Simultaneous direct and indirect calorimetry on normoxic and anoxic goldfish. J Exp Biol 142:325–335
van Waversveld J, Addink ADF, van den Thillart G, Smit H (1988) Direct calorimetry on free swimming goldfish at different oxygen levels. J Therm Anal 33:1019–1026
Vornanen M, Stecyk JAW, Nilsson G (2009) The anoxia-tolerant crucian carp (Carassius carassius L.). In: Richards JG, Farrell AP, Brauner CJ (eds) Hypoxia. Elsevier, San Diego
Wang T, Lefevre S, Houng DTT, Van Cong N, Bayley M (2009) Impacts of hypoxia on growth and digestion. In: Richards JG, Farrell AP, Brauner CJ (eds) Hypoxia. Elsevier, San Diego
White WT, Hall NG, Potter IC (2002) Reproductive biology and growth during pre- and postnatal life of Trygonoptera personata and T. mucosa (Batoidea: Urolophidae). Mar Biol 140:699–712
Wieser W, Krumschnabel G (2001) Hierarchies of ATP-consuming processes: direct compared with indirect measurements, and comparative aspects. Biochem J 355:389–395
Wourms JP (1972a) Developmental biology of annual fishes. 1. Stages in normal development of Austrofundulus myersi Dahl. J Exp Zool 182:143–168
Wourms JP (1972b) Developmental biology of annual fishes. 3. Pre-embryonic and embryonic diapause of variable duration in eggs of annual fishes. J Exp Zool 182:389–414
Wu RSS (2009) Effects of hypoxia on fish reproduction and development. In: Richards JG, Farrell AP, Brauner CJ (eds) Hypoxia. Elsevier, San Diego
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2010 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Richards, J.G. (2010). Metabolic Rate Suppression as a Mechanism for Surviving Environmental Challenge in Fish. 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_6
Download citation
DOI: https://doi.org/10.1007/978-3-642-02421-4_6
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-02420-7
Online ISBN: 978-3-642-02421-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)