Skip to main content

The Connection Between Oxidative Stress and Estivation in Gastropods and Anurans

  • Chapter
  • First Online:
Aestivation

Abstract

In situations of food and water deprivation associated with unfavorable environmental conditions, a number of animal species undergo estivation. This state of locomotor inactivity involves a drastic reduction in the metabolic rate, allowing the estivator to survive long periods of adverse situations. However, the arousal from dormancy causes a rapid increase in oxygen consumption, which may elevate the production of oxygen radicals. Thus, it is expected that animals that arouse from estivation suffer a physiological oxidative stress. The reported mechanisms that protect estivators (anurans and gastropods) from the potential dangers of increased oxyradical formation are discussed. This includes the modulation of endogenous antioxidant defenses (enzymes and glutathione) of gastropods during dormancy, preparing them for arousal. A different strategy used for estivating anurans is also discussed.

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

Access this chapter

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

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

    CAS  PubMed  Google Scholar 

  • Adelman R, Saul RL, Ames BN (1988) Oxidative damage to DNA; relation to species, metabolic rate and life span. Proc Natl Acad Sci USA 85:2706–2708

    Article  CAS  PubMed  Google Scholar 

  • Augusto O (2006) Radicais Livres: Bons, maus e naturais. Oficina de Textos, São Paulo

    Google Scholar 

  • Bailey SER (1981) Circannual and circadian rhythms in the snail Helix aspersa Müller and the photoperiodic control of annual activity and reproduction. J Comp Physiol 142:89–94

    Article  Google Scholar 

  • Barnhart MC (1986) Respiratory gas tensions and gas exchange in active and dormant land snails Otala lactea. Physiol Zool 59:733–745

    Google Scholar 

  • Barnhart MC, McMahon BR (1987) Discontinuous carbon dioxide release and metabolic depression in dormant land snails. J Exp Biol 128:123–138

    Google Scholar 

  • Belló-Klein A, Morgan-Martins MI, Barp J, Llesuy S, Belló AA, Singal PK (2000) Circannual changes in antioxidants and oxidative stress in the heart and liver in rats. Comp Biochem Physiol C 126:203–208

    Article  Google Scholar 

  • Bemis WE, Burggren WW, Kemp NE (1987) In: Bemis WE, Burggren WW, Kemp NE (eds) The biology and evolution of lungfish. Alan R. Liss, New York

    Google Scholar 

  • Bickler PE, Buck LT (2007) Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annu Rev Physiol 69:145–170

    Article  CAS  PubMed  Google Scholar 

  • Bishop T, Brand MD (2000) Processes contributing to metabolic depression in hepatopancreas cells from the snail Helix aspersa. J Exp Biol 203:3603–3612

    CAS  PubMed  Google Scholar 

  • Bishop T, St-Pierre J, Brand MD (2002) Primary causes of decreased mitochondrial oxygen consumption during metabolic depression in snail cells. Am J Physiol Regul Integr Comp Physiol 282:R372–R382

    CAS  PubMed  Google Scholar 

  • Boyer BB, Barnes BM, Lowell BB, Grujic D (1998) Differential regulation of uncoupling protein gene homologues in multiple tissues of hibernating ground squirrels. Am J Physiol 275:R1232–R1238

    CAS  PubMed  Google Scholar 

  • Brand MD (2000) Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Exp Gerontol 35:811–820

    Article  CAS  PubMed  Google Scholar 

  • Buzadzic B, Spasic MB, Saicic ZS, Radojicic R, Petrovic VM, Halliwell B (1990) Antioxidant defenses in the ground squirrel Citellus citellus: 2. The effect of hibernation. Free Radic Biol Med 9:407–413

    Article  CAS  PubMed  Google Scholar 

  • Brookes PS, Buckingham JA, Tenreiro AM, Hulbert AJ, Brand MD (1998) The proton permeability of the inner membrane of liver mitochondria from ectothermic and endothermic vertebrates and from obese rats: correlations with standard metabolic rate and phospholipid fatty acid composition. Comp Biochem Physiol B 119:325–334

    Article  CAS  PubMed  Google Scholar 

  • Caldeira da Silva CC, Cerqueira FM, Barbosa LF, Medeiros MH, Kowaltowski AJ (2008) Mild mitochondrial uncoupling in mice affects energy metabolism, redox balance and longevity. Aging Cell 7:552–560

    Article  CAS  PubMed  Google Scholar 

  • Caputa M, Nowakowska A, Rogalska J, Wentowska K (2005) Winter torpor in Helix pomatia: regulated defence mechanism or forced inactivity? Can J Zool 83:1608–1613

    Article  Google Scholar 

  • Cardoso LA (2005) Metabolismo de radicais livres em peixes tolerantes a baixas tensões de oxigênio. PhD thesis, Universidade de Brasília

    Google Scholar 

  • Carey HV, Rhoads CA, TY AW (2003) Hibernation induces glutathione redox imbalance in ground squirrel intestine. J Comp Physiol B 173:269–276

    Article  CAS  PubMed  Google Scholar 

  • Chown SL, Storey KB (2006) Linking molecular physiology to ecological realities. Physiol Biochem Zool 79:314–323

    Article  CAS  PubMed  Google Scholar 

  • David E, Tanguy A, Pichavant K, Moraga D (2005) Response of the Pacific oyster Crassostrea gigas to hypoxia exposure under experimental conditions. FEBS J 272:5635–5652

    Article  CAS  PubMed  Google Scholar 

  • Ferreira MVR, Alencastro ACR, Hermes-Lima M (2003) Role of antioxidant defenses during estivation and anoxia exposure in freshwater snails Biomphalaria tenagophila (Orbigny, 1835). Can J Zool 81:1239–1248

    Article  CAS  Google Scholar 

  • Ferreira-Cravo M, Piedras FR, Moraes TB, Ferreira JLR, Freitas DPS, Machado MD, Geracitano LA, Monserrat JM (2007) Antioxidant responses and reactive oxygen species generation in different body regions of the estuarine polychaeta Laeonereis acuta (Nereididae). Chemosphere 66:1367–1374

    Article  CAS  PubMed  Google Scholar 

  • Furtado-Filho OV, Polcheira C, Machado DP, Mourão G, Hermes-Lima M (2007) Selected oxidative stress markers in a South American crocodilian species. Comp Biochem Physiol C 146:241–254

    Article  Google Scholar 

  • González-Flecha B, Demple B (1995) Metabolic sources of hydrogen peroxide in aerobically growing Escherichia coli. J Biol Chem 270:13681–13687

    Article  PubMed  Google Scholar 

  • Grundy JE, Storey KB (1998) Antioxidant defenses and lipid peroxidation damage in estivating toads, Scaphiopus couchii. J Comp Physiol B 169:132–142

    Article  Google Scholar 

  • Guppy M, Reeves DC, Bishop T, Withers P, Buckingham JA, Brand MD (2000) Intrinsic metabolic depression in cells isolated from the hepatopancreas of estivating snails. FASEB J 14:999–1004

    CAS  PubMed  Google Scholar 

  • Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. University Press, Oxford

    Google Scholar 

  • Harper ME, Green K, Brand MD (2008) The efficiency of cellular energy transduction and its implications for obesity. Annu Rev Nutr 28:13–33

    Article  CAS  PubMed  Google Scholar 

  • Hermes-Lima M (2004) Oxygen in biology and biochemistry: role of free radicals. In: Storey KB (ed) Functional metabolism: regulation, and adaptation. Wiley, New York, pp 319–368

    Google Scholar 

  • Hermes-Lima M, Storey KB (1995a) Antioxidant defenses and metabolic depression in a pulmonate land snail. Am J Physiol 268:R1386–R1393

    CAS  PubMed  Google Scholar 

  • Hermes-Lima M, Storey KB (1995b) Xanthine oxidase and xanthine dehydrogenase from an estivating land snail. Z Naturforsch 50C:685–694

    Google Scholar 

  • Hermes-Lima M, Zenteno-Savín T (2002) Animal response to drastic changes in oxygen availability and physiological oxidative stress. Comp Biochem Physiol C 133:537–556

    Article  Google Scholar 

  • Hermes-Lima M, Storey JM, Storey KB (1998) Antioxidant defenses and metabolic depression. The hypothesis of preparation for oxidative stress in land snails. Comp Biochem Physiol B 120:437–448

    Article  CAS  PubMed  Google Scholar 

  • Hermes-Lima M, Storey JM, Storey KB (2001) Antioxidant defenses and animal adaptation to oxygen availability during environmental stress. In: Storey KB, Storey JM (eds) Cell and molecular responses to stress, vol 2. Elsevier Science, Amsterdan, pp 263–287

    Google Scholar 

  • Herreid CF (1977) Metabolism of land snails (Otala lactea) during dormancy, arousal and activity. Comp Biochem Physiol A 56:211–215

    Article  PubMed  Google Scholar 

  • Hudson NJ, Lehnert SA, Ingham AB, Symonds B, Franklin CE, Harper GS (2006) Lessons from an estivating frog: sparing muscle protein despite starvation and disuse. Am J Physiol 290:R836–R843

    CAS  Google Scholar 

  • Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA (2007) Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev 87:1175–1213

    Article  CAS  PubMed  Google Scholar 

  • Iglesias J, Santos M, Castillejo J (1996) Annual activity cycles of the land snail Helix aspersa müller in natural populations in north-western Spain. J Moll Stud 62:495–505

    Article  Google Scholar 

  • Jastroch M, Buckingham JA, Helwig M, Klingenspor M, Brand MD (2007) Functional characterisation of UCP1 in the common carp: uncoupling activity in liver mitochondria and cold-induced expression in the brain. J Comp Physiol B 177:743–752

    Article  CAS  PubMed  Google Scholar 

  • Keller M, Sommer AM, Pörtner HO, Abele A (2004) Seasonality of energetic functioning and production of reactive oxygen species by lugworm (Arenicola marina) mitochondria exposed to acute temperature changes. J Exp Biol 207:2529–2538

    Article  CAS  PubMed  Google Scholar 

  • Livingstone DR, de Zwaan A (1983) Carbohydrate metabolism in gastropods. In: Wilbur KM (ed) The mollusca, vol 1. Academic, New York, pp 177–242

    Google Scholar 

  • Lushchak VI, Bagnyukova TV, Lushchak OV, Storey JM, Storey KB (2005) Hypoxia and recovery perturb free radical processes and antioxidant potential in common carp (Cyprinus carpio) tissues. Int J Biochem Cell Biol 37:1319–1330

    Article  CAS  PubMed  Google Scholar 

  • McClanahan L (1967) Adaptations of the spadefoot toad, Scaphiopus couchii, to desert environments. Comp Biochem Physiol 20:73–79

    Article  CAS  Google Scholar 

  • Michaelidis B (2002) Studies on the extra- and intracellular acid-base status and its role on metabolic depression in the land snail Helix lucorum (L.) during estivation. J Comp Physiol B 172:347–354

    Article  CAS  PubMed  Google Scholar 

  • Niyogi S, Biswas S, Sarker S, Datta AG (2001) Seasonal variation of antioxidant and biotransformation enzymes in barnacle, Balanus balanoides, and their relation with polyaromatic hydrocarbons. Mar Environ Res 52:13–26

    Article  CAS  PubMed  Google Scholar 

  • Nowakowska A, Swiderska-Kolacz G, Rogalska J, Caputa M (2009) Effect of winter torpor upon antioxidative defence in Helix pomatia. Can J Zool 87:471–479

    Article  CAS  Google Scholar 

  • Orr AL, Lohse LA, Drew KL, Hermes-Lima M (2009) Physiological oxidative stress after arousal from hibernation in arctic ground squirrel. Comp Biochem Physiol A 153:213–221

    Article  Google Scholar 

  • Page MM, Peters CW, Staples JF, Stuart JA (2009) Intracellular antioxidant enzymes are not globally upregulated during hibernation in the major oxidative tissues of the 13-lined ground squirrel Spermophilus tridecemlineatus. Comp Biochem Physiol A 152:115–122

    Article  Google Scholar 

  • Pamenter ME, Richards MD, Buck LT (2007) Anoxia-induced changes in reactive oxygen species and cyclic nucleotides in the painted turtle. J Comp Physiol B 177:473–481

    Article  CAS  PubMed  Google Scholar 

  • Paraense WL (1986) Distribução dos caramujos no Brasil. In: Reis FA, Faria II, Katz N (eds) Modernos sonhecimentos sobre esquistossomose mansônica, Academia Mineira de Medicina. Anais da Academia Mineira de Medicina, Belo Horizonte, pp 117–128

    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 B 166:375–381

    Article  CAS  PubMed  Google Scholar 

  • Philipp E, Pörtner HO, Abele D (2005) Mitochondrial ageing of a polar and a temperate mud clam. Mech Ageing Dev 126:610–619

    Article  CAS  PubMed  Google Scholar 

  • Pinder AW, Storey KB, Ultsch GR (1992) Estivation and hibernation. In: Feder ME, Burggren WW (eds) Environmental biology of the Amphibia. University of Chicago Press, Chicago, pp 250–274

    Google Scholar 

  • Ramnanan CJ, Storey KB (2006) Glucose-6-phosphate dehydrogenase regulation during hypometabolism. Biochem Biophys Res Commun 339:7–16

    Article  CAS  PubMed  Google Scholar 

  • Ramnanan CJ, Groom AG, Storey KB (2007) Akt and its downstream targets play key roles in mediating dormancy in land snails. Comp Biochem Physiol B 148:245–255

    Article  PubMed  Google Scholar 

  • Ramnanan CJ, Allan ME, Groom AG, Storey KB (2009) Regulation of global protein translation and protein degradation in aerobic dormancy. Mol Cell Biochem 323:9–20

    Google Scholar 

  • Ramos-Vasconcelos GR (2005) Metabolismo de radicais livres em gastrópodes terrestres. PhD thesis, Universidade de Brasília

    Google Scholar 

  • Ramos-Vasconcelos GR, Hermes-Lima M (2003) Hypometabolism, antioxidant defenses and free radical metabolism in the pulmonate land snail Helix aspersa. J Exp Biol 206:675–685

    Article  CAS  PubMed  Google Scholar 

  • Ramos-Vasconcelos GR, Cardoso LA, Hermes-Lima M (2005) Seasonal modulation of free radical metabolism in estivating land snails Helix aspersa. Comp Biochem Physiol C 140:165–174

    Article  Google Scholar 

  • Ramsey JJ, Hagopian K, Kenny TM, Koomson EK, Bevilacqua L, Weindruch R, Harper ME (2004) Proton leak and hydrogen peroxide production in liver mitochondria from energy-restricted rats. Am J Physiol Endocrinol Metab 286:E31–E40

    Article  CAS  PubMed  Google Scholar 

  • Rees BB, Hand SC (1993) Biochemical correlates of estivation tolerance in the mountainsnail Oreohelix (Pulmonata: Oreohelicidae). Biol Bull 184:230–242

    Article  Google Scholar 

  • Rey B, Sibille B, Romestaing C, Belouze M, Letexier D, Servais S, Barre H, Duchamp C, Voituron Y (2008) Reptilian uncoupling protein: functionality and expression in sub-zero temperatures. J Exp Biol 211:1456–1462

    Article  CAS  PubMed  Google Scholar 

  • Rolfe DF, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758

    CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Sies H (1986) Biochemistry of oxidative stress. Angew Chem Int Ed Engl 25:1058–1071

    Article  Google Scholar 

  • Speakman JR, Talbot DA, Selman C, Snart S, Mclaren JS, Redman P, Krol E, Jackson DM, Johnson MS, Brand MD (2004) Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 3:87–95

    Article  CAS  PubMed  Google Scholar 

  • Storey KB (1996) Oxidative stress: animal adaptations in nature. Braz J Med Biol Res 29:1715–1733

    CAS  PubMed  Google Scholar 

  • Storey KB (2002) Life in the slow lane: molecular mechanisms of estivation. Comp Biochem Physiol A 133:733–754

    Article  Google Scholar 

  • Storey KB (2003) Mammalian hibernation. Transcriptional and translational controls. Adv Exp Med Biol 543:21–38

    CAS  PubMed  Google Scholar 

  • Storey KB (2006) Gene hunting in hypoxia and exercise. In: Roach RC, Hackett PH, Wagner PD (eds) Hypoxia and exercise, advances in experimental medicine and biology, vol 588. Springer, New York, pp 293–309

    Google Scholar 

  • Storey KB, Storey JM (2009) Metabolic regulation and gene expression during aestivation. A chapter in this book

    Google Scholar 

  • St-Pierre J, Brand MD, Boutilier RG (2000) The effect of metabolic depression on proton leak rate in mitochondria from hibernating frogs. J Exp Biol 203:1469–1476

    CAS  PubMed  Google Scholar 

  • Stuart JA, Gillis TE, Ballantyne JS (1998) Compositional correlates of metabolic depression in the mitochondrial membranes of estivating snails. Am J Physiol 275:R1977–R1982

    CAS  PubMed  Google Scholar 

  • Teles HMS, Marques CCD (1989) Estivation of Biomphalaria tenagophila (Pulmonata, Planorbidae). Rev Saude Publica 23:76–78

    CAS  PubMed  Google Scholar 

  • Turrens JF, Freeman BA, Levitt JG, Crapo JD (1982) The effect of hyperoxia on superoxide production by lung submitochondrial particles. Arch Biochem Biophys 217:401–410

    Article  CAS  PubMed  Google Scholar 

  • Voituron Y, Servais S, Romestaing C, Douki T, Barré H (2006) Oxidative DNA damage and antioxidant defenses in the European common lizard (Lacerta vivipara) in supercooled and frozen states. Cryobiology 52:74–82

    Article  CAS  PubMed  Google Scholar 

  • Vorhaben JE, Klotz AV, Campbell JW (1984) Activity and oxidative metabolism of the land snail Helix aspersa. Physiol Zool 57:357–365

    CAS  Google Scholar 

  • Welker AF (2009) Efeitos da flutuação da disponibilidade de oxigênio e da privação alimentar sobre o metabolismo de radicais livres. PhD thesis, Universidade de São Paulo, Brazil

    Google Scholar 

  • Wieser W, Wright E (1979) The effects of season and temperature on D-lactate dehydrogenase, pyruvate kinase and arginase kinase in the foot of Helix pomatia L. Hoppe-Seyler’s Z Physiol Chem 360:533–542

    CAS  PubMed  Google Scholar 

  • Wilhelm Filho D, Torres MA, Tribess TB, Pedrosa RC, Soares CHL (2001a) Influence of season and pollution on the antioxidant defenses of the cichlid fish acará (Geophagus brasiliensis). Braz J Med Biol Res 34:719–726

    Article  CAS  PubMed  Google Scholar 

  • Wilhelm Filho D, Tribess T, Gáspari C, Claudio FD, Torres MA, Magalhães ARM (2001b) Seasonal changes in antioxidant defenses of the digestive gland of the brown mussel (Perna perna). Aquaculture 203:149–158

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from CNPq, Brazil (Projeto Universal) and CNPq-Instituto do Milênio (Projeto Redoxoma). M. Hermes-Lima and M. Ferreira-Cravo were recipients of Fellowships from CNPq and CAPES (Brazil), respectively. A.F. Welker was granted a leave of absence from his teaching duties at UFG, Catalão, to work in this manuscript. The authors thank Dr. Ken Storey (Carleton University, Ottawa) for critical reading of this manuscript. This work is dedicated to Mrs. Eneida S. Hermes – former elementary school teacher – on the occasion of her 90th birthday on September 19, 2009.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marcelo Hermes-Lima .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Ferreira-Cravo, M., Welker, A.F., Hermes-Lima, M. (2010). The Connection Between Oxidative Stress and Estivation in Gastropods and Anurans. 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_3

Download citation

Publish with us

Policies and ethics