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.
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REFERENCES
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
Bara, G., Location of steroid hormone production in the ovary of Trachurus mediterraneus, Acta. Histochem., 1974, vol. 51, pp. 90−101.
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
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.
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
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.
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
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
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
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.
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.
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
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
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
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
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.
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
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
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
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
Mousa, M.A., Biological studies on the repreoduction of mullet (Mugil cephalus L.) in Egypt, Ph.D. Thesis, Ain Shams University, 1994.
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.
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
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
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
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
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.
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
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
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
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
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
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
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
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.
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
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
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
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
Valdebenito, I., Paiva, L., and Berland, M., Follicular atresia in teleost fish: A review, Arch. Med. Vet., 2011, vol. 43, pp. 11–25.
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
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
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
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
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We are extremely grateful to Professor Shaaban Mousa (Klinik fur Anaesthesiologie, Charite-Uńiversitatsmedi-zin Berlin) for critical review of the manuscript.
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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.
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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
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DOI: https://doi.org/10.1134/S0032945223030104