Skip to main content
Log in

Description of the Sex Hormone-Secreting Cells during Oocyte Development and Atresia in Flathead Grey Mullet Mugil cephalus (Mugilidae) in Al-Bardawil Lagoon, Egypt

  • Published:
Journal of Ichthyology Aims and scope Submit manuscript

Abstract

The present study described the changes of steroidogenic cells accompanied the ovarian maturation in flathead grey mullet, Mugil cephalus, from Al-Bardawil lagoon. Here, five periods of ovarian development including previtellogenesis, vitellogenesis (early, mid, and late), and pre-spawning ones were successfully obtained from mullet female inhabiting Al-Bardawill lagoon. In addition, abnormal feature of atresia was noticed in the vitellogenic stages of the ovaries. In atretic follicles, the granulosa cells converted into active phagocytic cells digesting and consuming the yolk in those oocytes. The histochemical and ultrastructural observations showed that the follicular cells, theca and granulosa of the developing oocytes are the site of the sex hormones synthesis. Both theca and granulosa have manifested both quantitative and qualitative alterations concomitant during oogenesis as reflected by an obvious increase in number, size, and content of lipid droplets of those cells. In conclusion, the present observations show the histological and ultrastructural changes of steroidogenic cells during ovarian maturation and atresia of the grey mullet. This new information is essential for managing and preserving Al-Bardawil lagoon as a natural source of mullet broodstock and for achieving sustainable development for this fish.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.

Similar content being viewed by others

REFERENCES

  1. Azoury, R. and Eckstein, B., Steroid production in the ovary of the gray mullet (Mugil cephalus) during stages of egg ripening, Gen. Comp. Endocrinol., 1980, vol. 42, pp. 244–250. https://doi.org/10.1016/0016-6480(80)90194-x

    Article  CAS  PubMed  Google Scholar 

  2. Bara, G., Location of steroid hormone production in the ovary of Trachurus mediterraneus, Acta. Histochem., 1974, vol. 51, pp. 90−101.

    CAS  PubMed  Google Scholar 

  3. Berchtold, J.P., Ultracytochemical demonstration and probable localization of 3β-hydroxysteroid dehydrogenase activity with a ferricyanide technique, Histochemistry, 1977, vol. 50, pp. 175−190. https://doi.org/10.1007/bf00491065

    Article  CAS  PubMed  Google Scholar 

  4. Bose, S., Alterations in histoarchitecture and ultrastructure of the ovary of brackish-water grey mullet Liza parsia (Hamilton) during different reproductive phases, Int. J. Res. Anal. Rev., 2019, vol. 6, no. 1, pp. 934−942.

    Google Scholar 

  5. Choi, J.S., Shin, S.R., Kim, H.J., et al., Gonadal abnormality and intersexuality of Oplegnathus fasciatus (Teleostei: Oplegnathidae) collected from the southern coast of Korea: A case report, Devel. Reprod., 2021, vol. 25, no. 3, pp. 123–131. https://doi.org/10.12717/DR.2021.25.3.123

  6. Christensen, A.K. and Gillim, S.W., The correlation of fine structure and function in steroid-secreting cells, with emphasis on those of the gonads, in The Gonads, Mckerns, K.W., Ed., N.Y.: Appleton-Century Crofts, 1969, pp. 415−488.

    Google Scholar 

  7. Cox, T.L., Guy, C.S., Holmquist, L.M., and Webb, M.A.H., Reproductive indices and observations of mass ovarian follicular atresia in hatchery-origin pallid sturgeon, J. Appl. Ichthyol., 2022, vol. 38, pp. 391–402. https://doi.org/10.1111/jai.14339

    Article  Google Scholar 

  8. Das, P., Maiti, A., and Maiti, B.R., Circannual changes in morphological, ultrastructural and hormonal activities of the ovary of an estuarine grey mullet, Mugil cephalus L., Biol. Rhythm Res., 2013, vol. 44, no. 4, pp. 541−567. https://doi.org/10.1080/09291016.2012.721588

    Article  CAS  Google Scholar 

  9. Emel’yanova, N.G., Pavlov, D.A., Pavlov, E.D., et al., Anomalies in ovarian condition of manybar goatfish Parupeneus multifasciatus (Mullidae) from the coastal zone of South Central Vietnam, J. Ichthyol., 2014, vol. 54, no. 1, pp. 76−84. https://doi.org/10.1134/S0032945214010056

    Article  Google Scholar 

  10. González-Kother, P., Oliva, M.E., Tanguy, A., and Moraga, D., A review of the potential genes implicated in follicular atresia in teleost fish, Marine Gen., 2020, vol. 50, Article 100704.

  11. https://doi.org/10.1016/j.margen.2019.100704

  12. Greeley, M.S., Jr., Calder, D.R., and Wallace, R.A., Oocyte growth and development in the striped mullet Mugil cephalus during seasonal ovarian recrudescence: Relationship to fecundity and size at maturity, Fish Bull., 1987, vol. 85, pp. 187−200.

    Google Scholar 

  13. Hinsch, G.W., Ovary of golden crab, Chaceon fenneri: I. Post-spawning and oosorption, J. Morphol., 1992, vol. 211, pp. 1−6. https://doi.org/10.1002/jmor.1052110102

    Article  PubMed  Google Scholar 

  14. Kagawa, H., Ultrastructure and histochemical observations regarding the ovarian follicles of the amago salmon (Oncorhynchus rhodurus), J. Univ. Occupat. Environ. Health, 1985, vol. 7, pp. 27−35. https://doi.org/10.7888/juoeh.7.27

    Article  CAS  Google Scholar 

  15. Kagawa, H., Takano, K., and Nagahama, Y., Correlation of plasma estradiol-17β and progesterone levels with ultrastructure and histochemistry of ovarian follicles in the white-spotted Char, Salvelinus leucomaenis, Cell Tiss. Res., 1981, vol. 218, pp. 315−329. https://doi.org/10.1007/BF00210347

    Article  CAS  Google Scholar 

  16. Kagawa, H., Young, G., and Nagahama, Y., Relationship between seasonal plasma estradiol-17β and testosterone levels and in vitro production by ovarian follicles of amago salmon (Oncorhynchus rhodurus), Biol. Reprod., 1983, vol. 29, pp. 301−309. https://doi.org/10.1095/biolreprod29.2.301

    Article  CAS  PubMed  Google Scholar 

  17. Kim, S.J., Lee, Y.D., Yeo, I.K., et al., Reproductive cycle of the female grey mullet, Mugil cephalus, on the coast of Jeju Island, Korea, J. Environ. Toxicol., 2004, vol. 19, no. 1, pp. 73–80.

    Google Scholar 

  18. Kurosumi, K. and Fujita, H., An Atlas of Electron Micrographs. Functional Morphology of Endocrine Glands, Tokyo: Lgaku Shoin Ltd., 1974. https://doi.org/10.1002/food.19770210529

  19. Lang, I., Electron microscopic and histochemical investigations of the atretic oocyte of Perca fluviatilis L. (Teleostei), Cell Tiss. Res., 1981, vol. 220, pp. 201−212. https://doi.org/10.1007/BF00209978

    Article  CAS  Google Scholar 

  20. Matsuyama, M., Nagahama, Y., and Matsuura, S., Observation on ovarian follicle ultrastructure in the marine teleost, Pagrus major, during vitellogenesis and oocyte maturation, Aquaculture, 1991, vol. 92, pp. 67−82. https://doi.org/10.1016/0044-8486(91)90009-V

    Article  Google Scholar 

  21. McDermott, S.F., Maslenikov, K.P., and Gunderson, D.R., Annual fecundity, batch fecundity, and oocyte atresia of Atka mackerel (Pleurogrammus monopterygius) in Alaskan waters, Fish. Bull., 2007, vol. 105, pp. 19−29. http://hdl.handle.net/1834/25546

    Google Scholar 

  22. Mousa, M.A., Biological studies on the repreoduction of mullet (Mugil cephalus L.) in Egypt, Ph.D. Thesis, Ain Shams University, 1994.

  23. Mousa, M.A., The efficacy of clove oil as an anaesthetic during the induction of spawning of thin-lipped grey mullet, Liza ramada (Risso), J. Egypt. Ger. Soc. Zool., 2004, vol. 45, no. A, pp. 515−535.

  24. Mousa, M.A., Induced spawning and embryonic development of Liza ramada reared in freshwater ponds, An. Reprod. Sci., 2010, vol. 119, pp. 115–122. https://doi.org/10.1016/j.anireprosci.2009.12.014

    Article  Google Scholar 

  25. Nagahama, Y., 17α, 20 β-Dihydroxy-4-pregnen.3-one: A teleost maturation-inducing hormone, Devel. Growth Differ., 1987, vol. 29, pp. 1−12. https://doi.org/10.1111/j.1440-169X.1987.00001.x

    Article  CAS  Google Scholar 

  26. Nagahama, Y., Clarke, W.C., and Hoar, W.S., Ultrastructure of putative steroid- producing cells in the gonads of coho (Oncorhynchus kisutch) and pink salmon (Oncorhynchus gorbuscha), Can. J. Zool., 1978, vol. 56, pp. 2508−2519. https://doi.org/10.1139/z78-339

    Article  Google Scholar 

  27. Óskarsson, G.J. and Taggart, C.T., Fecundity variation in Icelandic summer-spawning herring and implications for reproductive potential, ICES J. Marine Sci., 2006, vol. 63, no. 3, pp. 493−503. https://doi.org/10.1016/j.icesjms.2005.10.002

    Article  Google Scholar 

  28. Oven, L.S., Resorption of vitellogenous oocytes as an indicator of the state of the Black Sea fish populations and their environment, J. Ichthyol., 2004, vol. 44, no. 1, pp. 115−119.

    Google Scholar 

  29. Pavlov, E.D., Tunb, N.V., and Tu, N.T.H., State of gonads in juvenile triploid trout Oncorhynchus mykiss under conditions of South Vietnam after artificial sex inversion, Ibid., 2010, vol. 50, no. 8, pp. 650−659. https://doi.org/10.1134/S0032945210080102

    Article  Google Scholar 

  30. Privalikhin, A.M., Zhukova, K.A., and Poluektova, O.G., Atresia of developing oocytes in walleye pollock Theragra chalcogramma, Ibid., 2015, vol. 55, no. 5, pp. 664−670. https://doi.org/10.1134/S0032945215050136

    Article  Google Scholar 

  31. Reynolds, E.S., Staining of tissue sections for electron microscopy with heavy metals, J. Cell Biol., 1963, vol. 17, pp. 208−212. https://doi.org/10.1083/jcb.17.1.208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Rideout, R.M. and Tomkiewicz, J., Skipped spawning in fishes: More common than you might think, Marine Coast. Fish. 2011, vol. 3, no. 1, pp. 176−189. https://doi.org/10.1080/19425120.2011.556943

    Article  Google Scholar 

  33. Rosenblum, P.M., Pudney, J., and Callard, L.P., Gonadal morphology, enzyme, histochemistry and palsma steroid levels during the annual reproductive cycle of male and female brown bulhead catfish, Ictalurus nebulosus Lesueur, J. Fish Biol., 1987, vol. 31, pp. 325−341. https://doi.org/10.1111/j.1095-8649.1987.tb05239.x

    Article  CAS  Google Scholar 

  34. Rzepkowska, M., Adamek-Urbańska, D., Fajkowska, M., and Roszko, M.Ł., Histological evaluation of gonad impairments in Russian sturgeon (Acipenser gueldenstaedtii) reared in re-circulating aquatic system (RAS), Animals, 2020, vol. 10, no. 8, Article 1439. https://doi.org/10.3390/ani10081439

    Article  PubMed  PubMed Central  Google Scholar 

  35. Selvaraj, S., Chidambaram, P., Ezhilarasi, V., et al., A review on the reproductive dysfunction in farmed finfish, Ann. Res. Rev. Biol., 2021, vol. 36, no. 10, pp. 65−81. https://doi.org/10.9734/ARRB/2021/v36i1030437

    Article  Google Scholar 

  36. Senarat, S., Poolprasert, P., Kettratad, J., et al., Ultrastructure of ovarian follicles and testis in zebra-snout seahorse Hippocampus barbouri (Jordan & Richardson, 1908) under aquaculture conditions, J. Adv. Veterinar. Res., 2021, vol. 11, no. 1, pp. 47−53.

    Google Scholar 

  37. Shireman, J., Gonadal development of striped mullet Mugil cephahus in freshwater, Prog. Fish Cult., 1975, vol. 37, pp. 205−208. https://doi.org/10.1577/1548-8659(1975)37[205:GDOSMM]2.0.CO;2

    Article  Google Scholar 

  38. Sueiro, M.C., Palacios, M.G., Trudeau, V.L., et al., Anthropogenic impact on the reproductive health of two wild Patagonian fish species with differing reproductive strategies, Sci, Total Environ., 2022, vol. 838, no. 2, Article 155862. https://doi.org/10.1016/j.scitotenv.2022.155862

    Article  CAS  PubMed  Google Scholar 

  39. Suzuki, K., Asahina, K., Tamaru, C.S., et al., Biosynthesis of 17α, 20β-Dihydroxy-4-pregnen-3- one in the ovaries of grey mullet (Mugil cephalus) during induced ovulation by carp pituitary homogenates and an LHRH analogue, Gen. Comp. Endocrinol., 1991, vol. 84, pp. 215−221. https://doi.org/10.1016/0016-6480(91)90044-7

    Article  CAS  PubMed  Google Scholar 

  40. Thiaw, O.T. and Mattei, X., Natural degenerating mitochondria in ovarian follicles of a cyprinodontidae fish, Epiplatys spilargvreus (Teleost), Mol. Reprod. Devel., 1992, vol. 32, pp. 67−72. https://doi.org/10.1002/mrd.1080320111

    Article  CAS  PubMed  Google Scholar 

  41. Valdebenito, I., Paiva, L., and Berland, M., Follicular atresia in teleost fish: A review, Arch. Med. Vet., 2011, vol. 43, pp. 11–25.

    Article  CAS  Google Scholar 

  42. Van den Hurk, R. and Peute, J., Cyclic changes in the ovary of the rainbow trout, Salmo gairdneri, with special reference to sites of steroidogenesis, Cell Tiss. Res., 1979, vol. 199, pp. 289−306. https://doi.org/10.1007/bf00236140

    Article  CAS  Google Scholar 

  43. Vélez-Arellano, N., Sánchez-Cárdenas, R., Salcido-Guevara, L.A., et al., Gonadal development, sex ratio, and length at sexual maturity of white mullet Mugil curema (Actinopterygii: Mugilidae) inhabiting southeastern Gulf of California, Lat. Am. J. Aquat. Res., 2022, vol. 50, no. 3, Article 2817. https://doi.org/10.3856

    Google Scholar 

  44. Yaron, Z., Observations on the granulosa cells of Acanthobrama terrae-sanctae and Tilapia nilotica (Teleostei), Gen. Comp. Endocrinol., 1971, vol. 17, pp. 247−252. https://doi.org/10.1016/0016-6480(71)90132-8

    Article  CAS  PubMed  Google Scholar 

  45. Yang, Y., Wang, G., Li, Y., et al., Oocytes skipped spawning through atresia is regulated by somatic cells revealed by transcriptome analysis in Pampus argenteus, Front. Mar. Sci., 2022, vol. 9, Article 927548. https://doi.org/10.3389/fmars.2022.927548

    Article  Google Scholar 

Download references

ACKNOWLEDGMENTS

We are extremely grateful to Professor Shaaban Mousa (Klinik fur Anaesthesiologie, Charite-Uńiversitatsmedi-zin Berlin) for critical review of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. A. Mousa.

Ethics declarations

Conflict of interest. The authors declare that they have no conflict of interest.

Statement on the welfare of humans or animals. Fish handling was revised and confirmed by the Committee for Institutional Care of Aquatic Organisms and Experimental Animals at National Institute of Oceanography and Fisheries (Certificate number or code: NIOF-AQ5-F-22-R-020). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mousa, M.A., El-Messady, F.A. & Khalil, N.A. Description of the Sex Hormone-Secreting Cells during Oocyte Development and Atresia in Flathead Grey Mullet Mugil cephalus (Mugilidae) in Al-Bardawil Lagoon, Egypt. J. Ichthyol. 63, 513–523 (2023). https://doi.org/10.1134/S0032945223030104

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0032945223030104

Keywords:

Navigation