Skip to main content
SpringerLink
Log in

Physiological responses to acute experimental hypoxia in the air-breathing Indian catfish, Clarias batrachus (Linnaeus, 1758)

  • Published:
Journal of Biosciences Aims and scope Submit manuscript

Abstract

With an aim to study the mechanism of adaptation to acute hypoxic periods by hypoxia-tolerant catfish, Clarias batrachus, the mass-specific metabolic rate (VO2) along with its hematological parameters, metabolic response and antioxidant enzyme activities were studied. During progressive hypoxia, C. batrachus was found to be an oxyconformer and showed a steady decline in its aquatic oxygen consumption rate. When C. batrachus was exposed for different periods at experimental hypoxia level (0.98 ± 0.1 mg/L, DO), hemoglobin and hematocrit concentrations were increased, along with decrease in mean cellular hemoglobin concentration, which reflected a physiological adaptation to enhance oxygen transport capacity. Significant increase in serum glucose and lactate concentration as well as lactate dehydrogenase activity was observed. Antioxidant enzymes were found to operate independently of one another, while total glutathione concentration was unaffected in any of the tissues across treatments. These observations suggested that hypoxia resulted in the development of oxidative stress and C. batrachus was able to respond through increase in the oxygen carrying capacity, metabolic depression and efficient antioxidant defense system to survive periods of acute hypoxia.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8

Similar content being viewed by others

References

  • Assendelft OW and England JM 1982 Advances in hematological methods—the blood count (Boca Raton, FL: CRC Press)

    Google Scholar 

  • Baker PJ, Costanzo JP and Lee RE Jr 2007 Oxidative stress and antioxidant capacity of a terrestrially hibernating hatchling turtle. J. Comp. Physiol. B. 177 875–883

    Article  PubMed  CAS  Google Scholar 

  • Braun N, De Lima RL, Moraes B, Loro VL and Baldisserotto B 2006 Survival, growth and biochemical parameters of silver catfish, Rhamdia quelen (Quoy & Gaimard, 1824), juveniles exposed to different dissolved oxygen levels. Aqua. Res. 37 1524–1531

    Article  CAS  Google Scholar 

  • Cech JJ 1990 Respirometry; in Methods of fish biology (eds) CB Schreck and PB Moyle (Bethesda MD: American Fisheries Society) pp 335–362

    Google Scholar 

  • Chonder SL 1999 Biology of finfish and shellfish (Howrah, India: SCSC Publisher) pp 303–313

    Google Scholar 

  • Cooper RU, Clough LM, Farwell MA and West TL 2002 Hypoxia-induced metabolic and antioxidant enzymatic activities in the estuarine fish Leiostomus xanthurus. J. Exp. Mar. Biol. Ecol. 279 1–20

    Article  CAS  Google Scholar 

  • Dacie SIV and Lewis SM 1991 Practical haematology 7th edition (London, Melborne and New York: J.A. Chuchill Ltd. Livingstone)

    Google Scholar 

  • Damotharan P, Perumal NV, Arumugam M, Vijayalakshmi S and Balasubramanian T 2010 Seasonal variation of physico-chemical characteristics in point calimere coastal waters south east coast of India. Middle East J. Sci. Res. 64 333–339

    Google Scholar 

  • Dean B 1912 Additional notes on the living specimens of the Australian lungfish Ceratodus forsteri, in the collection of the Zoological Society of London. Proc. Zool. Soc. London. 82 607–612

  • de Graaf G and Janssen H 1996 Artificial reproduction and pond rearing of the African catfish, Clarias gariepinus in sub-Saharan Africa. (Amsterdam: Nesfisco Foundation)

    Google Scholar 

  • Fernandes MN and Mazon AF 2003 Environmental pollution and fish gill morphology; in Fish adaptations (eds) AL Val and BG Kapoor (Enfield: Science Publishers) pp 203–231

    Google Scholar 

  • Garg TK and Mittal AK 1990 The epidermal and inner epithelial lining of the operculum in Clarias batrachus Clariidae, Siluriformes. Jap. J. Icthy. 37 149–157

    Google Scholar 

  • Graham JB 1997 Air-breathing fishes: Evolution, diversity and adapatation (San Diego, CA: Academic Press)

    Google Scholar 

  • Henriksson P, Mandic M and Richards JG 2008 The osmo-respiratory compromise in sculpins: impaired gas exchange is associated with freshwater tolerance. Physiol. Biochem. Zool. 81 310–319

    Article  PubMed  Google Scholar 

  • Hochachka PW and Somero GN 2002 Biochemical adaptation: mechanism and process in physiological evolution (Oxford: Oxford University Press) p 466

    Google Scholar 

  • Ishimatsu A, Hayashi M and Kikkawa T 2008 Fishes in high-CO2, acidified oceans. Mar. Ecol. Prog. Ser. 373 295–302

    Article  CAS  Google Scholar 

  • Lai AY and Todd KG 2006 Hypoxia-activated microglial mediators of neuronal survival are differentially regulated by tetracyclines. Glia 53 809–816

    Article  PubMed  Google Scholar 

  • Lushchak VI 2011 Environmentally induced oxidative stress in aquatic animals. Aquat. Toxicol. 101 13–30

    Article  PubMed  CAS  Google Scholar 

  • Lushchak VI and Bagnyukova TV 2006 Effects of different environmental oxygen levels on free radical processes in fish. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 144 283–289

    Article  PubMed  Google Scholar 

  • Lushchak VI and Bagnyukova TV 2007 Hypoxia induces oxidative stress in tissues of a goby, the rotan Perccottus glenii. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 148 390–7

    Article  PubMed  Google Scholar 

  • Lushchak VI, Bagnyukova TV, Lushchak OV, Storey JM and 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  PubMed  CAS  Google Scholar 

  • Martinez ML, Landry C, Boehm R, Manning S, Cheek AO and Rees BB 2006 Effects of long-term hypoxia on enzymes of carbohydrate metabolism in the Gulf killifish, Fundulus grandis. J. Exp. Biol. 209 3851–3861

    Article  PubMed  CAS  Google Scholar 

  • Martinez ML, Raynard EL, Bernard BR and Chapman LJ 2011 Oxygen limitation and tissue metabolic potential of the African fish Barbus neumayeri: roles of native habitat and acclimatization. BMC Ecol. 11 2

    Article  PubMed  CAS  Google Scholar 

  • McKenzie DJ, Steffensen JF, Korsmeyer K, Whiteley NM, Bronzi P and Taylor EW 2007 Swimming alters responses to hypoxia in the Adriatic sturgeon Acipenser naccarii J. Fish Biol. 70 651–658

    Article  CAS  Google Scholar 

  • Mohindra V, Tripathi RK, Singh A and Singh B 2012 Molecular characterization and expression analysis of a novel cystatin-like gene in a hypoxia-tolerant Indian catfish, Clarias batrachus [Linnaeus, 1758]. Fish Shellfish Immunol. DOI: 10.1016/j.fsi.2012.11.018

  • Munshi JSD and Ghosh TK 1994 Metabolic wheel hypothesis as applied to air-breathing fishes of India; in Advances in fish biology (ed) HR Singh (Delhi: Hindustan Publishing Corporation) pp 70–78

    Google Scholar 

  • Mustafa SA, Al-Subiai SN, Davies SJ and Jha AN 2011 Hypoxia-induced oxidative DNA damage links with higher level biological effects including specific growth rate in common carp, Cyprinus carpio L. Ecotoxicol. 20 1455–1466

    Article  CAS  Google Scholar 

  • Mustafa SA, Davies SJ and Jha AN 2012 Determination of hypoxia and dietary copper mediated sub-lethal toxicity in carp, Cyprinus carpio, at different levels of biological organization. Chemosphere 87 413–422

    Article  PubMed  CAS  Google Scholar 

  • Nilsson GE and Lutz PL 1993 Role of GABA in hypoxia tolerance, metabolic depression and hibernation–possible links to neurotransmitter evolution. Comp. Biochem. Physiol. C 105 329–336

    Article  PubMed  CAS  Google Scholar 

  • Nilsson L, Kogure K and Busto R 1975 Effects of hypothermia and hyperthermia on brain energy metabolism. Acta Anaesth. Scand. 193 199–205

    Article  Google Scholar 

  • Nilsson S and Grove DG 1974 Adrenergic and cholinergic innervation of the spleen of the cod: Gadus morhua. Eur. J. Pharmacol. 28 135–143

    Article  PubMed  CAS  Google Scholar 

  • Oruc EO and Uner N 2000 Combined effects of 2, 4-D and azinphosmethyl on antioxidant enzymes and lipid peroxidation in liver of Oreochromis niloticus. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 127 291–296

    PubMed  CAS  Google Scholar 

  • Perry SF and Reid SG 1994 The effects of acclimation temperature on the dynamics of catecholamine release during acute hypoxia in the rainbow trout Oncorhynchus mykiss. J. Exp. Biol. 186 289–307

    PubMed  CAS  Google Scholar 

  • Portner HO, Heisler N and Grieshaber MK 1985 Oxygen consumption and mode of energy production in the intertidal worm Sipunculus nudus L: Definition and characterization of the critical PO2 for an oxyconformer. Res. Physiol. 59 361–377

    Article  CAS  Google Scholar 

  • Saha N and Ratha BK 2007 Functional ureogenesis and adaptation to ammonia metabolism in Indian freshwater air-breathing catfishes. Fish Physiol. Biochem. 33 283–295

    Article  CAS  Google Scholar 

  • Saint-Paul U 1984 Physiological adaptation to hypoxia of a neotropical characoid fish Colossoma macropomum, Serrasalmidae. Env. Biol. Fishes. 11 53–62

    Article  Google Scholar 

  • Speers-Roesch B, Brauner CJ, Farrell AP, Hickey AJR, Renshaw GMC, Wang YS and Richards JG 2012 Hypoxia tolerance in elasmobranchs. II. Cardiovascular function and tissue metabolic responses during progressive and relative hypoxia exposures. J Exp. Biol. 215 103–114

    Article  PubMed  CAS  Google Scholar 

  • Staples JF and Buck LT 2009 Matching cellular metabolic supply and demand in energy-stressed animals. Comp. Biochem. Physiol. A 153 95–105

    Google Scholar 

  • Timmerman CM and Chapman LJ 2004 Behavioral and Physiological Compensation for Chronic Hypoxia in the Sailfin Molly (Poecilia latipinna). Physiol. Biochem. Zool. 77 601–610

    Article  PubMed  Google Scholar 

  • Trachootham D, Lu W, Ogasawara MA, Valle NRD and Huang P 2008 Redox regulation of cell survival. Antioxid. Redox Signal 10 1343–1374

    Article  CAS  Google Scholar 

  • Urbina MA and Glover CN 2012 Should I stay or should I go? Physiological, metabolic and biochemical consequences of voluntary emersion upon aquatic hypoxia in the scaleless fish Galaxias maculatus. J. Comp. Physiol. B DOI: 10.1007/s00360-012-0678-3

  • Urbina MA, Glover CN and Forster ME 2012 A novel oxyconforming response in the freshwater fish Galaxias maculatus. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 161 301–306

    Article  PubMed  CAS  Google Scholar 

  • Welker AF, Campos EG, Cardoso LA and Hermes-Lima M 2012 Role of catalase on the hypoxia/reoxygenation stress in the hypoxia-tolerant Nile tilapia. Am. J. Physiol. Regu. Physiol. 302 1111–1118

    Google Scholar 

  • Wells RMG and Weber RE 1991 Is there an optimal haematocrit for rainbow trout, Oncorhynchus mykiss Walbaum? An interpretation of recent data based on blood viscosity measurements. J. Fish. Biol. 38 53–65

    Article  Google Scholar 

  • Wilhelm-Filho D, Torres MA, Zaniboni-Filho E and Pedrosa RC 2005 Effect of different oxygen tensions on weight gain, feed conversion, and antioxidant status in piapara, Leporinus elongates Valenciennes, 1847. Aquaculture 244 349–357

    Article  Google Scholar 

  • Willmore WG and Storey KB 1997 Antioxidant systems and anoxia tolerance in a freshwater turtle Trachemys scripta elegans. Mol. Cell Biochem. 170 177–185

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was carried out under National Agricultural Innovation Project ‘Bio-prospecting of Genes and Allele Mining for Abiotic Stress Tolerance’, and financial support provided by NAIP-Indian Council of Agricultural Research is duly acknowledged.

Author information

Authors and Affiliations

  1. National Bureau of Fish Genetic Resources, Canal Ring Road, P.O. Dilkusha, Lucknow, 226 001, India

    Ratnesh Kumar Tripathi, Vindhya Mohindra, Akanksha Singh, Rajesh Kumar & Joy Krushna Jena

  2. Awadhesh Pratap Singh University, Rewa, 486 001, India

    Rahasya Mani Mishra

Authors
  1. Ratnesh Kumar Tripathi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vindhya Mohindra
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Akanksha Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rajesh Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rahasya Mani Mishra
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Joy Krushna Jena
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vindhya Mohindra.

Additional information

Corresponding editor: STUART A NEWMAN

MS received 05 November 2012; accepted 15 January 2013

Corresponding editor: Stuart A Newman

[Tripathi RK, Mohindra V, Singh A, Kumar R, Mishra RM and Jena JK 2013 Physiological responses to acute experimental hypoxia in the air-breathing Indian catfish, Clarias batrachus (Linnaeus, 1758). J. Biosci. 38 1–11] DOI 10.1007/s12038-013-9304-0

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tripathi, R.K., Mohindra, V., Singh, A. et al. Physiological responses to acute experimental hypoxia in the air-breathing Indian catfish, Clarias batrachus (Linnaeus, 1758). J Biosci 38, 373–383 (2013). https://doi.org/10.1007/s12038-013-9304-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12038-013-9304-0

Keywords

Search

Navigation