Fish Physiology and Biochemistry

, Volume 43, Issue 6, pp 1677–1688 | Cite as

Diel cyclic hypoxia alters plasma lipid dynamics and impairs reproduction in goldfish (Carassius auratus)

  • Aritra Bera
  • Paramita Banerjee Sawant
  • Subrata Dasgupta
  • N. K. Chadha
  • Bhawesh T. Sawant
  • Asim Kumar Pal


Diel cyclic hypoxia occurs with varying frequency and duration in freshwater habitats, yet little is known about its effects on reproduction of freshwater fishes. The present study shows that long-term exposure of goldfish (Carassius auratus) to cyclic hypoxia (0.8 ± 0.2 mg/l dissolved oxygen) for 9 h or more, per day, altered plasma lipid and sex steroid profiles, which in turn directly or indirectly suppressed ovarian growth and viable spermatozoa production. Hypoxia decreased total cholesterol and high density lipoprotein (HDL p < 0.05) and elevated triglycerides (TG; p < 0.05) in both sexes. Plasma steroid concentrations particularly of 17α-hydroxyprogesterone (17-HP), estradiol (E2), testosterone (T) in females, and T and 11-ketotestosterone (11-KT) in males were attenuated under diel hypoxic conditions. Intriguingly, both diel and continuous hypoxia elevated plasma E2 and vitellogenin levels in males. However, neither lipid nor steroid profiles recorded any variation in a dose-dependent manner in response to diel hypoxia. The reduced GSI, decreased number of tertiary oocytes, and motile spermatozoa in hypoxic fish clearly indicate suppression of gametogenesis. Thereby, prolonged diel cyclic hypoxia may affect valuable fishery resources and fish population structure by impairing reproductive performances and inducing estrogenic effects in males.


Hypoxia Diel cycle Steroids Lipids Reproduction Goldfish 



The authors are thankful to the Director and Vice Chancellor, Central Institute of Fisheries Education, Mumbai, for providing necessary facilities. The first author acknowledges the Indian Council of Agricultural Research, New Delhi, for the Junior Research Fellowship.


  1. Babin PJ, Vernier JM (1989) Plasma lipoproteins in fish. J Lipid Res 30(503):467–489PubMedGoogle Scholar
  2. Bozkurt Y (2006) Relationship between body condition and spermatological properties in goldfish (Carassius auratus) semen. J Anim Vet Adv 5:423–425Google Scholar
  3. Byrne BM, Gruber MA, Ab G (1989) The evolution of egg yolk proteins. Prog Biophys Mol Biol 53(1):33–69CrossRefPubMedGoogle Scholar
  4. Clayton DA (1993) Mudskippers. In: Ansell AD, Gibson RN, Barnes M (eds) Oceanography and marine biology: an annual review. University College London Press, London, pp 507–577Google Scholar
  5. De Angelis C, Ferri C, Urbani L, Farrace S (1996) Effect of acute exposure to hypoxia on electrolytes and water metabolism regulatory hormones. Aviat Space Environ Med 67(8):746–750PubMedGoogle Scholar
  6. Fradette C, Souich PD (2004) Effect of hypoxia on cytochrome P450 activity and expression. Curr Drug Metab 5(3):257–271CrossRefPubMedGoogle Scholar
  7. Gillet C, Breton B, Billard R (1978) Seasonal effects of exposure to temperature and photoperiod regimes on gonad growth and plasma gonadotropin in goldfish (Carassius auratus). Ann Biol Anim Biochi Biophys 18(4):1045–1049CrossRefGoogle Scholar
  8. Glazar AI, Mullen SF, Liu J, Benson JD, Critser JK, Squires EL, Graham JK (2009) Osmotic tolerance limits and membrane permeability characteristics of stallion spermatozoa treated with cholesterol. Cryobiology 59(2):201–206CrossRefPubMedGoogle Scholar
  9. Gwynne JT, Strauss JF III (1982) The role of lipoproteins in steroidogenesis and cholesterol metabolism in steroidogenic glands. Endocr Rev 3(3):299–329CrossRefPubMedGoogle Scholar
  10. Heath AG (1995) Water pollution and fish physiology, 2nd edn. CRC press, FloridaGoogle Scholar
  11. Henderson RJ, Tocher DR (1987) The lipid composition and biochemistry of freshwater fish. Prog Lipid Res 26(4):281–347CrossRefPubMedGoogle Scholar
  12. Hochachka P, Somero G (2002) Biochemical adaption. Oxford University Press, New YorkGoogle Scholar
  13. Jeong JY, Kwon HB, Ahn JC, Kang D, Kwon SH, Park JA, Kim KW (2008) Functional and developmental analysis of the blood–brain barrier in zebrafish. Brain Res Bull 75(5):619–628CrossRefPubMedGoogle Scholar
  14. Kavlock RJ (1999) Overview of endocrine disruptor research activity in the United States. Chemosphere 39(8):1227–1236CrossRefPubMedGoogle Scholar
  15. Kobayashi M, Aida K, Hanyu I (1987) Hormone changes during ovulation and effects of steroid hormones on plasma gonadotropin levels and ovulation in goldfish. Gen Comp Endocrinol 67(1):24–32CrossRefPubMedGoogle Scholar
  16. Kruger JD, Smit GL, Vuren JH, Ferreira JT (1984) Some chemical and physical characteristics of the semen of Cyprinus carpio L. and Oreochromis mossambicus (Peters). J Fish Biol 24(3):263–272CrossRefGoogle Scholar
  17. Landry CA, Steele SL, Manning S, Cheek AO (2007) Long term hypoxia suppresses reproductive capacity in the estuarine fish, Fundulus grandis. Comp Biochem Physiol A Mol Integr Physiol 148(2):317–323CrossRefPubMedGoogle Scholar
  18. Ljubić BB, Aladrović J, Marenjak TS, Laškaj R, Majić-Balić I, Milinković-Tur S (2009) Cholesterol concentration in seminal plasma as a predictive tool for quality semen evaluation. Theriogenology 72(8):1132–1140CrossRefGoogle Scholar
  19. Lutz PL, Nilsson GE, Perez-Pinzon MA (1996) Anoxia tolerant animals from a neurobiological perspective. Comp Biochem Physiol 113:3–13CrossRefGoogle Scholar
  20. Luzio A, Matos M, Santos D, Fontaínhas-Fernandes AA, Monteiro SM, Coimbra AM (2016) Disruption of apoptosis pathways involved in zebrafish gonad differentiation by 17α-ethinylestradiol and fadrozole exposures. Aquat Toxicol 177:269–284CrossRefPubMedGoogle Scholar
  21. Mandic M, Lau GY, Nijjar MM, Richards JG (2008) Metabolic recovery in goldfish: a comparison of recovery from severe hypoxia exposure and exhaustive exercise. Comp Biochem Physiol Part C: Toxicol Pharmacol 148(4):332–338Google Scholar
  22. Martinovic D, Villeneuve DL, Kahl MD, Blake LS, Brodin JD, Ankley GT (2009) Hypoxia alters gene expression in the gonads of zebrafish (Danio rerio). Aquat Toxicol 95(4):258–272CrossRefPubMedGoogle Scholar
  23. Mocé E, Purdy PH, Graham JK (2010) Treating ram sperm with cholesterol-loaded cyclodextrins improves cryosurvival. Anim Reprod Sci 118(2):236–247CrossRefPubMedGoogle Scholar
  24. Nikinmaa M, Rees BB (2005) Oxygen-dependent gene expression in fishes. Am J Phys Regul Integr Comp Phys 288(5):R1079–R1090Google Scholar
  25. Pederson RC (1988) Cholesterol biosynthesis, storage, and mobilization in steroidogenic organs. In: Yeagle PL (ed) Biology of cholesterol. CRC Press, Boca RatonGoogle Scholar
  26. Perchec G, Jeulin C, Cosson J, Andre F, Billard R (1995) Relationship between sperm ATP content and motility of carp spermatozoa. J Cell Sci 108(2):747–753PubMedGoogle Scholar
  27. Richards JG, Farraell AP, Brauner CJ (eds) (2009) Hypoxia, 1st edn. Academic Press, LondonGoogle Scholar
  28. Saroglia M, Terova G, Stradis A, Caputo A (2002) Morphometric adaptations of sea bass gills to different dissolved oxygen partial pressures. J Fish Biol 60(6):1423–1430CrossRefGoogle Scholar
  29. Schreck CB, Hopwood ML (1974) Seasonal androgen and estrogen patterns in the goldfish, Carassius auratus. Trans Am Fish Soc 103(2):375–378CrossRefGoogle Scholar
  30. Schulz RW, De França LR, Lareyre JJ, LeGac F, Chiarini-Garcia H, Nobrega RH, Miura T (2010) Spermatogenesis in fish. Gen Comp Endocrinol 165(3):390–411CrossRefPubMedGoogle Scholar
  31. Scott AP (1987) Reproductive endocrinology of fish. Plenum Press, New YorkCrossRefGoogle Scholar
  32. Shang EH, Yu RM, Wu RS (2006) Hypoxia affects sex differentiation and development, leading to a male-dominated population in zebrafish (Danio rerio). Environ Sci Technol 40(9):3118–3122CrossRefPubMedGoogle Scholar
  33. Sharpe RL, MacLatchy DL (2007) Lipid dynamics in goldfish (Carassius auratus) during a period of gonadal recrudescence: effects of β-sitosterol and 17β-estradiol exposure. Comp Biochem Physiol Part C: Toxicol Pharmacol 145(4):507–517Google Scholar
  34. Sharpe RL, Drolet M, MacLatchy DL (2006) Investigation of de novo cholesterol synthetic capacity in the gonads of goldfish (Carassius auratus) exposed to the phytosterol beta-sitosterol. Reprod Biol Endocrinol 4(1):1CrossRefGoogle Scholar
  35. Smith VH (2003) Eutrophication of freshwater and coastal marine ecosystems a global problem. Environ Sci Pollut Res 10(2):126–139CrossRefGoogle Scholar
  36. Spanò L, Tyler CR, van Aerle R, Devos P, Mandiki SN, Silvestre F, Thomé JP, Kestemont P (2004) Effects of atrazine on sex steroid dynamics, plasma vitellogenin concentration and gonad development in adult goldfish (Carassius auratus). Aquat Toxicol 66(4):369–379CrossRefPubMedGoogle Scholar
  37. Sunyer RV, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. Proc Natl Acad Sci 105(40):15452–15457CrossRefGoogle Scholar
  38. Thillart VG (1982) Adaptations of fish energy metabolism to hypoxia and anoxia. Mol Physiol 2:49–61Google Scholar
  39. Thillart van den GU, van Waarde AR, Muller HJ, Erkelens CE, Addink AL, Lugtenburg JO (1989) Fish muscle energy metabolism measured by in vivo 31P-NMR during anoxia and recovery. Am J Phys Regul Integr Comp Phys 256(4):R922–R929Google Scholar
  40. Thomas P, Rahman MS (2009) Biomarkers of hypoxia exposure and reproductive function in Atlantic croaker: a review with some preliminary findings from the northern Gulf of Mexico hypoxic zone. J Exp Mar Biol Ecol 381:S38–S50CrossRefGoogle Scholar
  41. Thomas P, Rahman MS (2011) Extensive reproductive disruption, ovarian masculinization and aromatase suppression in Atlantic croaker in the northern Gulf of Mexico hypoxic zone. Proc R Soc Lond B Biol Sci. doi: 10.1098/rspb20110529
  42. Thomas P, Rahman MS, Kummer JA, Lawson S (2006) Reproductive endocrine dysfunction in Atlantic croaker exposed to hypoxia. Mar Environ Res 62:S249–S252CrossRefPubMedGoogle Scholar
  43. Thomas P, Rahman MS, Khan IA, Kummer JA (2007) Widespread endocrine disruption and reproductive impairment in an estuarine fish population exposed to seasonal hypoxia. Proc R Soc Lond B Biol Sci 274(1626):2693–2702CrossRefGoogle Scholar
  44. Thornton KW, Kimmel BL, Payne FE (1990) Reservoir limnology: ecological perspectives. Wiley, New YorkGoogle Scholar
  45. Tong Y, Shan T, Poh YK, Yan T, Wang H, Lam SH, Gong Z (2004) Molecular cloning of zebrafish and medaka vitellogenin genes and comparison of their expression in response to 17β-estradiol. Gene 328:25–36CrossRefPubMedGoogle Scholar
  46. Van Raaij MT, Van den Thillart GE, Vianen GJ, Pit DS, Balm PH, Steffens AB (1996) Substrate mobilization and hormonal changes in rainbow trout (Oncorhynchus mykiss, L.) and common carp (Cyprinus carpio, L.) during deep hypoxia and subsequent recovery. J Comp Physiol B 166(7):443–452CrossRefGoogle Scholar
  47. van der Meer DLM, van den Thillart GE,Witte F, de BakkerMA, Besser J, RichardsonMK, SpainkHP, Leito JT, Bagowski CP (2005) Gene expression profiling of the long-term adaptive response to hypoxia in the gills of adult zebrafish. Am J Phys Regul Integr Comp Phys 289(5):R1512–R1519Google Scholar
  48. Verma DK, Routray P, Dash C, Dasgupta S, Jena JK (2009) Physical and biochemical characteristics of semen and ultrastructure of spermatozoa in six carp species. Turk J Fish Aquat Sci 9(1):67–76Google Scholar
  49. Wang S, Yuen SS, Randall DJ, Hung CY, Tsui TK, Poon WL, Lai JC, Zhang Y, Lin H (2008) Hypoxia inhibits fish spawning via LH-dependent final oocyte maturation. Comp Biochem Physiol Part C: Toxicol Pharmacol 148(4):363–369Google Scholar
  50. Wise PM (2002) Estrogens and neuroprotection. Trends Endocrinol Metab 13(6):229–230CrossRefPubMedGoogle Scholar
  51. Wu RS, Zhou BS, Randall DJ, Woo NY, Lam PK (2003) Aquatic hypoxia is an endocrine disruptor and impairs fish reproduction. Environ Sci Technol 37(6):1137–1141CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Aritra Bera
    • 1
  • Paramita Banerjee Sawant
    • 2
  • Subrata Dasgupta
    • 3
  • N. K. Chadha
    • 2
  • Bhawesh T. Sawant
    • 4
  • Asim Kumar Pal
    • 2
  1. 1.Central Institute of Brackishwater Aquaculture (ICAR)ChennaiIndia
  2. 2.Fish Nutrition, Biochemistry and Physiology DivisionCentral Institute of Fisheries Education (ICAR)MumbaiIndia
  3. 3.Central Institute of Fisheries Education (ICAR), Kolkata CentreKolkataIndia
  4. 4.Taraporewala Marine Biological Research Station (KKV)MumbaiIndia

Personalised recommendations