Advertisement

Comparative Clinical Pathology

, Volume 27, Issue 4, pp 975–988 | Cite as

Seasonal modulation of reproductive hormones and related biomarkers in coldwater cyprinid Barilius bendelisis (Hamilton, 1807)

  • Neeraj Kumar SharmaEmail author
  • M. S. AkhtarEmail author
  • Ravindra Singh
  • N. N. Pandey
Original Article
  • 101 Downloads

Abstract

Barilius bendelisis is a valuable ornamental and food fish from India in which the endocrine control of its reproduction activity has not been widely reported. The present study was aimed to elucidate changes in serum endocrine hormones: 17β-estradiol (E2), testosterone (T), progesterone (P4), 17α, 20β-dihydroxyprogesterone (17α, 20β-P), cortisol (C), triiodothyronine (T3), and thyroxine (T4); aromatase activity (ARO), vitellogenin (VTG), and total antioxidant capacity (TAC) during different seasons of the year 2014. All studied parameters showed marked seasonal variations. The highest E2 level in males and females were recorded in winter (January) and rainy (September) seasons respectively. The T level exhibited dual peaks in both sexes, and the highest values were observed during the winter (January) and rainy (September) seasons. The serum levels of P4 and 17α, 20β-P during spring (March) and rainy (September) seasons were significantly higher and found associated with final sperm and oocyte maturation. The serum levels of ARO and VTG also showed bimodal pattern during the spring (March) and rainy (September) season and were well correlated with T and E2. Serum C level was detectable throughout the year in both sexes which were related to glucose metabolism and spawning events. Fluctuations in T3 and T4 levels were associated with somatic growth and reproduction events during different seasons in B. bendelisis. Serum TAC level was highest during summer (May and July) and autumn (November) seasons suggesting better antioxidant potential during these seasons. The study confirms that B. bendelisis is a multiple spawner with two spawning seasons.

Keywords

Barilius bendelisis Season Sex steroid hormones Aromatase Vitellogenin Multiple spawner 

Notes

Acknowledgements

The authors are grateful to the Director, ICAR Directorate of Coldwater Fisheries Research, Bhimtal-263136, Nainital, Uttarakhand and Head, Department of Zoology, HNB Garhwal Central University, Uttarakhand for providing necessary facilities and support to successfully carry out this study. This paper is a part of thesis research of the first author registered for PhD at HNB Garhwal University, Uttarakhand, India. The first author would also like to acknowledge University Grant Commission, India, for providing university fellowship during PhD tenure.

Electronic supplementary material

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

During all stages of our research, all applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Informed consent

Not applicable in this type of study.

References

  1. Adebiyi FA, Siraj SS, Harmin SA, Christianus A (2013) Plasma sex steroid hormonal profile and gonad histology during the annual reproductive cycle of river catfish Hemibagrus nemurus (Valenciennes, 1840) in captivity. Fish Physiol Biochem 39(3):547–557CrossRefPubMedGoogle Scholar
  2. Aggarwal N, Goswami SV, Khandelwal P, Sehgal N (2014) Aromatase activity in brain and ovary: seasonal variations correlated with circannual gonadal cycle in the catfish, Heteropneustes fossilis. Indian J Exp Biol 52:527–537PubMedGoogle Scholar
  3. Amer MA, Miura T, Miura C, Yamauchi K (2001) Involvement of sex steroid hormones in the early stages of spermatogenesis in Japanese huchen (Hucho perryi). Biol Reprod 65(4):1057–1066CrossRefPubMedGoogle Scholar
  4. Barannikova IA, Dyubin VP, Bayunova LV, Semenkova TB (2002) Steroids in the control of reproductive function in fish. Neurosci Behav Physiol 32(2):141–148CrossRefPubMedGoogle Scholar
  5. Barcellos LJ, Wassermann GF, Scott AP, Woehl VM, Quevedo RM, Ittzés I, Krieger MH, Lulhier F (2001) Steroid profiles in cultured female jundia, the siluridae Rhamdia quelen (Quoy and Gaimard, Pisces Teleostei), during the first reproductive cycle. Gen Comp Endocrinol 121(3):325–332CrossRefPubMedGoogle Scholar
  6. Berg AH, Westerlund L, Olsson PE (2004) Regulation of Arctic char (Salvelinus alpinus) egg shell proteins and vitellogenin during reproduction and in response to 17β-estradiol and cortisol. Gen Comp Endocrinol 135(3):276–285CrossRefPubMedGoogle Scholar
  7. Blanton ML, Specker JL (2007) The hypothalamic-pituitary-thyroid (HPT) axis in fish and its role in fish development and reproduction. Crit Rev Toxicol 37(1–2):97–115CrossRefPubMedGoogle Scholar
  8. Chaves-Pozo E, Arjona FJ, García-López A, García-Alcázar A, Meseguer J, García-Ayala A (2008) Sex steroids and metabolic parameter levels in a seasonal breeding fish (Sparus aurata L.) Gen Comp Endocrinol 156(3):531–536CrossRefPubMedGoogle Scholar
  9. Comeau LA, Campana SE (2006) Correlations between thyroidal and reproductive endocrine status in wild Atlantic cod. Can Tech Rep Fish Aquat Sci 2682Google Scholar
  10. Dobriyal AK, Singh HR (1987) The reproductive biology of a hill stream minor carp, Barilius bendelisis from Garhwal Himalaya, India. Vest Cs Spolec Zool 51:1–10Google Scholar
  11. Erel O (2004) A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem 37:277–285CrossRefPubMedGoogle Scholar
  12. Folmar LC, Denslow ND, Kroll K, Orlando EF, Enblom J, Marcino J, Metcalfe C, Guillette Jr LJ (2001) Altered serum sex steroids and vitellogenin induction in walleye (Stizostedion vitreum) collected near a metropolitan sewage treatment plant. Arch Environ Contam Toxicol 40(3):392–398CrossRefPubMedGoogle Scholar
  13. Fostier A, Jalabert B, Billard R, Breton B, Zohar Y (1983) The gonadal steroids. Fish Physiol 9:277–372CrossRefGoogle Scholar
  14. Heidari B, Roozati SA, Yavari L (2010) Changes in plasma levels of steroid hormones during oocyte development of Caspian Kutum (Rutilus frisii kutum, Kamensky, 1901). Anim Reprod 7(4):373–381Google Scholar
  15. Ismail MF, Siraj SS, Daud SK, Harmin SA (2011) Association of annual hormonal profile with gonad maturity of mahseer (Tor tambroides) in captivity. Gen Comp Endocrinol 170(1):125–130CrossRefPubMedGoogle Scholar
  16. Jarvis ET, Loke-Smith KA, Evans K, Kloppe RE, Young KA, Valle CF (2014) Reproductive potential and spawning periodicity in barred sand bass (Paralabrax nebulifer) from the San Pedro Shelf, southern California. Calif Fish Game 100(2):289–309Google Scholar
  17. Jobling S, Tyler CR (2003) Endocrine disruption in wild freshwater fish. Pure Appl Chem 75(11–12):2219–2234CrossRefGoogle Scholar
  18. Kadam DP, Suryakar AN, Ankush RD, Kadam CY, Deshpande KH (2010) Role of oxidative stress in various stages of psoriasis. Indian J Clin Biochem 25(4):388–392CrossRefPubMedPubMedCentralGoogle Scholar
  19. Larsson DJ, Mayer I, Hyllner SJ, Förlin L (2002) Seasonal variations of vitelline envelope proteins, vitellogenin, and sex steroids in male and female eelpout (Zoarces viviparus). Gen Comp Endocrinol 125(2):184–196CrossRefPubMedGoogle Scholar
  20. Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278CrossRefPubMedGoogle Scholar
  21. Liu J, Mai K, Xu W, Zhang Y, Zhou H, Ai Q (2015) Effects of dietary glutamine on survival, growth performance, activities of digestive enzyme, antioxidant status and hypoxia stress resistance of half-smooth tongue sole (Cynoglossus semilaevis Günther) post larvae. Aquaculture 446:48–56CrossRefGoogle Scholar
  22. Lubzens E, Young G, Bobe J, Cerdà J (2010) Oogenesis in teleosts: how fish eggs are formed. Gen Comp Endocrinol 165(3):367–389CrossRefPubMedGoogle Scholar
  23. Luty-Frackiewicz A, Markiewicz-Gorka I, Januszewska L (2006) Influence of smoking and alcohol consumption on total antioxidant status in patients with psoriasis. Adv Clin Exp Med 15(3):463–469Google Scholar
  24. Matozzo V, Gagné F, Marin MG, Ricciardi F, Blaise C (2008) Vitellogenin as a biomarker of exposure to estrogenic compounds in aquatic invertebrates: a review. Environ Int 34(4):531–545CrossRefPubMedGoogle Scholar
  25. Miura T, Miura C (2001) Japanese eel: a model for analysis of spermatogenesis. Zool Sci 18(8):1055–1063CrossRefGoogle Scholar
  26. Miura C, Higashino T, Miura T (2007) A progestin and an estrogen regulate early stages of oogenesis in fish. Biol Reprod 77(5):822–828CrossRefPubMedGoogle Scholar
  27. Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fisher 9(3):211–268CrossRefGoogle Scholar
  28. Mull CG, Lowe CG, Young KA (2010) Seasonal reproduction of female round stingrays (Urobatis halleri): steroid hormone profiles and assessing reproductive state. Gen Comp Endocrinol 166(2):379–387CrossRefPubMedGoogle Scholar
  29. Nagahama Y (1994) Endocrine regulation of gametogenesis in fish. Int J Dev Biol 38(2):217–229PubMedGoogle Scholar
  30. Nagahama Y, Yamashita M (2008) Regulation of oocyte maturation in fish. Develop Growth Differ 50:195–219CrossRefGoogle Scholar
  31. Nash JP, Davail-Cuisset B, Bhattacharyya S, Suter HC, Le Menn F, Kime DE (2000) An enzyme linked immunosorbant assay (ELISA) for testosterone, estradiol, and 17, 20β-dihydroxy-4-pregenen-3-one using acetylcholinesterase as tracer: application to measurement of diel patterns in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 22(4):355–363CrossRefGoogle Scholar
  32. Nautiyal P, Negi RS (2004) Population structure, dietary resources utilization and reproductive strategies of sympatric Barilius bendelisis and Barilius vagra in lesser Himalayan mountain streams. 21th Century fish research, AJH. Publishing Corporation, Delhi 43–68Google Scholar
  33. Oo W (2002) Inland fisheries of the Union of Myanmar. In T Petr and DB Swar (eds.) Cold Water 441 Fisheries in the Trans-Himalayan Countries. FAO Fish Technical Paper, 431Google Scholar
  34. Pankhurst NW (2011) The endocrinology of stress in fish: an environmental perspective. Gen Comp Endocrinol 170(2):265–275CrossRefPubMedGoogle Scholar
  35. Peter MS (2011) The role of thyroid hormones in stress response of fish. Gen Comp Endocrinol 172(2):198–210CrossRefPubMedGoogle Scholar
  36. Raine JC (2011) Thyroid hormones and reproduction in fishes. In: Norris DO, Lopez KH (eds) Hormones and reproduction in vertebrates, volume 1-fishes. Elsevier academic press, London 83–95 ppGoogle Scholar
  37. Ray SN, Sinha RC (2014) Serum cortisol and glucose: reliable bioindicators of stress in the fish Labeo rohita. Int J Innov Sci Eng Technol 1:6–17Google Scholar
  38. Rice-Evans C, Miller NJ (1994) Total antioxidant status in plasma and body fluids. Methods Enzymol 234:279–293CrossRefPubMedGoogle Scholar
  39. Rinchard J, Kestemont P, Kuhn E, Fostier A (1993) Seasonal changes in plasma levels of steroid hormones in an asynchronous fish the gudgeon Gobio gobio L. (Teleostei, Cyprinidae). Gen Comp Endocrinol 92(2):168–178CrossRefPubMedGoogle Scholar
  40. Rolland RM (2000) A review of chemically-induced alterations in thyroid and vitamin A status from field studies of wildlife and fish. J Wildl Dis 36(4):615–635CrossRefPubMedGoogle Scholar
  41. 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
  42. Scott AP, Katsiadaki I, Witthames PR, Hylland K, Davies IM, McIntosh AD, Thain J (2006) Vitellogenin in the blood plasma of male cod (Gadus morhua): a sign of oestrogenic endocrine disruption in the open sea? Mar Environ Res 61(2):149–170CrossRefPubMedGoogle Scholar
  43. Scott AP, Sumpter JP, Stacey N (2010) The role of the maturation-inducing steroid, 17, 20β-dihydroxypregn-4-en-3-one, in male fishes: a review. J Fish Biol 76(1):183–224CrossRefPubMedGoogle Scholar
  44. Senthilkumaran B, Yoshikuni M, Nagahama Y (2004) A shift in steroidogenesis occurring in ovarian follicles prior to oocyte maturation. Mol Cell Endocrinol 215(1):11–18CrossRefPubMedGoogle Scholar
  45. Sharma NK, Akhtar MS, Pandey NN, Singh R, Singh AK (2017) Sex specific seasonal variation in hematological and serum biochemical indices of Barilius bendelisis from Central Himalaya, India. Proc Indian Acad Sci Sect B Biol Sci 87(4):1185–1197CrossRefGoogle Scholar
  46. Sisneros JA, Forlano PM, Knapp R, Bass AH (2004) Seasonal variation of steroid hormone levels in an intertidal-nesting fish, the vocal plainfin midshipman. Gen Comp Endocrinol 136(1):101–116CrossRefPubMedGoogle Scholar
  47. Słowińska M, Nynca J, Cejko BI, Dietrich MA, Horváth Á, Urbányi B, Kotrik L, Ciereszko A (2013) Total antioxidant capacity of fish seminal plasma. Aquaculture 20(400):101–104CrossRefGoogle Scholar
  48. Talwar PK, Jhingran AG (1991) Inland fishes of India and adjacent countries (Vols. 1 and 2). Oxford and IBH Publishing Co. Pvt. Ltd., New Delhi 1158–1215 ppGoogle Scholar
  49. Tilak R, Jaffer Z, Husain A (1984) Systematic status of Barilius bendelisis Hamilton (Cyprinidae: Pisces). Rec Zool Soc India 81(3–4):279–290Google Scholar
  50. Tricas TC, Maruska KP, Rasmussen LE (2000) Annual cycles of steroid hormone production, gonad development, and reproductive behavior in the Atlantic stingray. Gen Comp Endocrinol 118(2):209–225CrossRefPubMedGoogle Scholar
  51. Vazirzadeh A, Mojazi Amiri B, Fostier A (2014) Ovarian development and related changes in steroid hormones in female wild common carp (Cyprinus carpio carpio), from the south-eastern Caspian Sea. J Anim Physiol Anim Nutr 98(6):1060–1067CrossRefGoogle Scholar
  52. Venkataramanan R, Murali N, Sreekumar C, Gowrimanokari K (2016) Breeding tubercles in scales of male Barilius bendelisis (Hamilton, 1807) identified as sexual dimorphic character. Curr Sci 110(6):985Google Scholar
  53. Wisdom GB (1976) Enzyme-immunoassay. Clin Chem 22(8):1243–1255PubMedGoogle Scholar
  54. Young G, Kusakabe M, Nakamura I, Lokman PM, Goetz FW (2005) Gonadal steroidogenesis in teleost fish. In: N Sherwood and P Melamed (Eds) Molecular aspects of fish and marine biology. In: C, Hew (Ed.) Hormones and their Receptors in Fish Reproduction, Volume 2. World Scientific Publishing Co. Pvt. Ltd., Singapore, 155–223 pp.Google Scholar

Copyright information

© Springer-Verlag London Ltd., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Fish Nutrition and Physiology Laboratory, ICAR-Directorate of Coldwater Fisheries ResearchBhimtalIndia
  2. 2.Department of ZoologyHemwati Nandan Bahuguna Garhwal University, Tehri Campus BadshahithaulTehriIndia

Personalised recommendations