Abstract
The small yellow croaker Larimichthys polyactis is an economically important marine fish in Northeast Asia. Currently, its natural resources are threatened by overfishing and environmental pollution. Therefore, research on the reproductive system of the fish is crucial. Here, we studied the testis development and ultrastructural features of spermatogenesis in cultured L. polyactis using anatomical, histological, and ultrastructural techniques. A pair of testes, consisting of a central sperm duct and radial seminiferous lobules, were observed. The reproduction cycle of testes can be divided into stages I–VI. March to May was confirmed as the breeding season for male L. polyactis, while April is the ideal period for artificial breeding. The male L. polyactis can attain sexual maturity within 1 year. The spermatogenesis of L. polyactis comprised spermatogonium, spermatocyte, spermatid, and mature spermatozoon. The morphology of spermatogenic cells changed obviously during spermiogenesis, including nuclear shaping, midpiece and flagellum formation. The mature sperms consist of an ellipsoidal head, a short midpiece, and a long flagellum. The anterior of the head with a kidney-shaped nucleus can be distinguished. The midpiece is located posterior to the head and includes four to six spherical mitochondria. The flagellum has irregular lateral fins. The testis of L. polyactis is an unrestricted lobular type, with cystic spermatogenesis, type II spermiogenesis, and type II spermatozoa. These features are highly similar to those of other Sciaenid species. Our findings provide useful insights into the mechanism underlying testis development and spermatogenesis of L. polyactis, which can facilitate the artificial breeding of this species.
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Abascal, F., Medina, A., Megina, C., and Calzada, A., 2002. Ultrastructure of Thunnus thynnus and Euthynnus alletteratus spermatozoa. Journal of Fish Biology, 60(1): 147–153, DOI: https://doi.org/10.1006/jfbi.2001.1820.
Amikura, R., Kashikawa, M., Nakamura, A., and Kobayashi, S., 2001. Presence of mitochondria-type ribosomes outside mitochondria in germplasm of Drosophila embryos. Proceeding of the National Academy of Sciences, 98(16): 9133–9138, DOI: https://doi.org/10.1073/pnas.171286998.
Andrade, R. F., Bazzoli, N., Rizzo, E., and Sato, Y., 2001. Continuous gametogenesis in the neotropical freshwater teleost, Bryconops affinis (Pisces: Characidae). Tissue and Cell, 33(5): 524–532, DOI: https://doi.org/10.1054/tice.2001.0206.
Ashida, H., Tanabe, T., Satoh, K., Fukui, A., Tanaka, S., and Suzuki, N., 2010. Reproductive biology of male skipjack tuna Katsuwonus pelamis (Linnaeus) in the tropical western and central Pacific Ocean. Fisheries Science (Tokyo), 76(5): 785–793, DOI: https://doi.org/10.1007/s12562-010-0282-y.
Billard, R., Fostier, A., Weil, C., and Breton, B., 1982. Endocrine control of spermatogenesis in teleost fish. Canadian Journal of Fisheries & Aquatic Sciences, 39(1): 65–79, DOI: https://doi.org/10.1139/f82-009.
Brown-Peterson, N. J., Grier, H. J., and Overstreet, R. M., 2002. Annual changes in germinal epithelium determine male reproductive classes of the cobia. Journal of Fish Biology, 60(1): 178–202, DOI: https://doi.org/10.1006/jfbi.2001.1833.
Camargo, M. P., Cassel, M., Jesus, L. W. O., Nóbrega, R. H., and Borella, M. I., 2017. Characterization of undifferentiated spermatogonia and the spermatogonial niche in the lambari fish Astyanax altiparanae. Theriogenology, 96: 97–102, DOI: https://doi.org/10.1016/j.theriogenology.2017.03.027.
Chen, D. Y., Li, D., Ou, Y. M., Chen, B., and Ma, B. X., 2013. Gonadal structure observation in Ganchang hybrid crucian (Carassius cuvierius ♀ × Cyprinus carpio var. singuonensis ♂). Acta Hydrobiologica Sinica, 37(4): 698–704, DOI: https://doi.org/10.7541/2013.83.
Chen, R. Y., Lou, B., Zhan, W., Xu, D. D., Chen, L., and Liu, F., 2016. Broodstock cultivation and spawning induction techniques in small yellow croaker Pseudosciaena polyactis. Scientific Fish Farming, 35: 250–254, DOI: https://doi.org/10.16378/j.cnki.1003-1111.2016.03.010.
Chuma, S., Hosokawa, M., Tanaka, T., and Nakatsuji, N., 2009. Ultrastructural characterization of spermatogenesis and its evolutionary conservation in the germline: Germinal granules in mammals. Molecular and Cellular Endocrinology, 306(1–2): 17–23, DOI: https://doi.org/10.1016/j.mce.2008.11.009.
Cui, D., Liu, Z. W., Liu, N. X., Zhang, Y. Y., and Zhang, J. B., 2013. Histological study on the gonadal development of Scatophagus argus. Journal of Fisheries of China, 37(5): 696–704, DOI: https://doi.org/10.3724/SP.J.1231.2013.38442.
Fishelson, L., Delarea, Y., and Gon, O., 2006. Testis structure, spermatogenesis, spermatocytogenesis, and sperm structure in cardinal fish (Apogonidae, Perciformes). Anatomy & Embryology, 211(1): 31–46, DOI: https://doi.org/10.1007/s00429-005-0050-4.
Fu, S. Y., Jiang, J. H., Yang, W. X., and Zhu, J. Q., 2016. A histological study of testis development and ultrastructural features of spermatogenesis in cultured Acrossocheilus fasciatus. Tissue & Cell, 48(1): 49–62, DOI: https://doi.org/10.1016/j.tice.2015.10.005.
Guan, D. L., Huang, D. Q., and Huang, G. P., 1990. Cellular organization of the testis, spermatogenesis and spermiogenesis in goldfish (Carassius auratus). Acta Hydrobiologica Sinica, 14: 233–238, DOI: CNKI:SUN:SSWX.0.1990-03-004.
Guan, W. B., Wang, X. G., and Dai, X. J., 2011. Study on the reproductive characteristics of male big eye tuna (Thunnus obesus) from the East Pacific Ocean. Transactions of Oceanology and Limnology, 2011(4): 90–99, DOI: https://doi.org/10.13984/j.cnki.cn37-1141.2011.04.005.
Gusmao-Pompiani, P., Oliveira, C., and Quagio-Grassiotto, I., 2005. Spermatozoa ultrastructure in Sciaenidae and Polynemidae (Teleostei: Perciformes) with some consideration on Percoidei spermatozoa ultrastructure. Tissue & Cell, 37(3): 177–191, DOI: https://doi.org/10.1016/j.tice.2004.12.003.
Gwo, J. C., 1995. Spermatozoan ultrastructure of the teleost fish Acanthopagrus latus (Perciformes: Sparidae) with special reference to the basal body. Journal of Submicroscopic Cytology and Pathology, 27(3): 391–396.
Gwo, J. C., Gwo, H. H., and Chang, S. L., 1993. Ultrastructure of the spermatozoon of the teleost fish Acanthopagrus schlegeli (Perciformes: Sparidae). Journal of Morphology, 216(1): 29–33, DOI: https://doi.org/10.1002/jmor.1252160105.
Han, K. L., Le, M. H., An, C. M., Kim, S. Y., Park, M. S., and Chang, Y. J., 2010. Reproductive cycle of yellow croaker Larimichthys polyactis in southern waters off Korea. Fisheries Science, 76(6): 971–980, DOI: https://doi.org/10.1007/s12562-010-0288-5.
He, D. K., Chen, Y. F., and Cai, B., 2001. Histological studies on the gonad development of an endemic Tibet fish Gymnocypris selincuoensis. Acta Hydrobiologica Sinica, 25(1): 1–13, DOI: https://doi.org/10.3321/j.issn:1000-3207.2001.01.001.
Hu, M., Miao, L., Li, M. W., Zhang, H., Wang, J. H., and Wang, T. Z., 2014. Observation and comparison on the ultrastructure of the spermatozoon of Nibea albiflora and Pseudosciaena crocea. Journal of Biology, 31(2): 1–4, DOI: https://doi.org/10.3969/j.issn.2095-1736.2014.02.001.
Kang, H. W., Chung, E. Y., Chung, J. S., and Lee, K. Y., 2013. Ultrastructural studies of spermatogenesis and the functions of Leydig cells and Sertoli cells associated with spermatogenesis in Larimichthys polyactis (Teleostei, Perciformes, Sciaenidae). Animal Cells and Systems, 17(4): 250–258, DOI: https://doi.org/10.1080/19768354.2013.829783.
Lahnsteiner, F., and Patzner, R. A., 2008. Sperm morphology and ultrastructure in fish. In: Fish Spermatology. Alavi, S. M. H., et al., eds., Alpha Science Ltd., Oxford, UK, 1–61.
Liao, G. Y., Ou, Y. J., Li, J. E., Chen, C., and Zhuang, Z. M., 2011. Ultrastructure of spermatozoa in Epinephelus septemfasciatus. Journal of Shanghai Ocean University, 20(1): 71–75, DOI: https://doi.org/10.1016/S1671-2927(11)60313-1.
Lin, D. J., Zhang, J., Luo, J., Zheng, Z. Y., and Shi, X. W., 1992. Studies on the gonadal development and the annual reproductive cycle of the cultured large yellow croaker, Pseudosciaena crocea (Richardson). Journal of Fujian Normal University (Natural Science Edition), 8(3): 81–87.
Liu, B. J., Zhang, B. D., Gao, T. X., and Liu, J. X., 2017. Signatures of temporal genetic differentiation of the small yellow croaker (Larimichthys polyactis) revealed by microsatellite markers. Fisheries Research, 194: 50–54, DOI: https://doi.org/10.1016/j.fishres.2017.05.005.
Liu, F., Liu, Y. Y., Chu, T. Q., Lou, B., Zhan, W., and Chen, R. Y., 2019. Interspecific hybridization and genetic characterization of Larimichthys polyactis (♀) and L. crocea (♂). Aquaculture International, 27: 663–674, DOI: https://doi.org/10.1007/s10499-019-00353-x.
Liu, Y., 1993. Reproductive Physiology of Farmed Fish in China. 2nd edition. Chinese Agriculture Press, Beijing, 23–32.
Lou, Y. D., 1996. Histology and Embryology. 2nd edition. Chinese Agriculture Press, Beijing, 131–137.
Magalhaes, A. L. B., Andrade, R. F., Gomes, B. V. C., Perini, V. R., Rizzo, E., and Bazzoli, N., 2011. Ultrastructure of the semicystic spermatogenesis in the South American freshwater characid Hemigrammus marginatus (Teleostei, Characiformes). Journal of Applied Ichthyology, 27(4): 1041–1046, DOI: https://doi.org/10.1111/j.1439-0426.2011.01747.x.
Ma, S. L., Geng, Z., Xu, D. D., Lou, B., Mao, G. M., and Zhan, W., 2014. Histological observations on the gonadal development of Nibea albiflora. Journal of Zhejiang Ocean University (Natural Science), 33(2): 129–133, DOI: https://doi.org/10.3969/j.issn.1008-830X.2014.02.006.
Mattei, X., 1991. Spermatozoon ultrastructure and its systematic implications in fishes. Canadian Journal of Zoology, 69(12): 3038–3055, DOI: https://doi.org/10.1139/z91-428.
Mattei, X., Siau, Y., Thiaw, O. T., and Thiam, D., 1993. Peculiarities in the organization of testis of Ophidian sp. (Pisces Teleostei). Evidence for two types of spermatogenesis in teleost fish. Journal of Fish Biology, 43(6): 931–937, DOI: https://doi.org/10.1111/j.1095-8649.tb01167.x.
Meng, Q. W., Su, J. X., and Li, W. D., 1987. The Zootomy of Fishes. Shanghai Science and Technology Press, Shanghai, 263–265.
Miao, L., Li, M., Tang, X., Wang, T., Zhang, X. L., and Wang, T. Z., 2013. Sperm ultrastructure of Miichthys miiuy (Perciformes: Sciaenidae). The Israeli Journal of Aquaculture, 65(1): 842–848.
Parenti, L. R., and Grier, H. J., 2004. Evolution and phylogeny of gonad morphology in bony fishes. Integrative and Comparative Biology, 44(5): 333–348, DOI: https://doi.org/10.1093/icb/44.5.333.
Quagio-Grassiotto, I., Baicere-Silva, C. M., Santana, J., and Mirande, J. M., 2020. Spermiogenesis and sperm ultrastructure as sources of phylogenetic characters. The example of characid fishes (Teleostei: Characiformes). Zoologischer Anzeiger, 289: 77–86, DOI: https://doi.org/10.1016/j.jcz.2020.09.006.
Reunov, A. A., and Reunova, Y. A., 2016. Pre-meiotic transformation of germplasm-related structures during male gamete differentiation in Xenopus laevis. Zygote, 24(1): 42–47, DOI: https://doi.org/10.1017/s0967199414000690.
Schulz, R. W., França, L. R., Lareyre, J. J., Legac, F., Chiarini-Garcia, H., Nobrega, R. H., et al., 2010. Spermatogenesis in fish. General & Comparative Endocrinology, 165(3): 390–411, DOI: https://doi.org/10.1016/j.ygcen.2009.02.013.
Tang, D. J., Gao, X. M., Lin, C. W., Feng, B. B., Hou, C. C., and Zhu, J. Q., 2020. Cytological features of spermatogenesis in Opsariichthys bidens (Teleostei, Cyprinidae). Animal Reproduction Science, 222: 106608, DOI: https://doi.org/10.1016/j.anireprosci.2020.106608.
Wang, L., Liu, S. F., Zhuang, Z. M., Lin, H. R., and Meng, Z. N., 2015. Mixed-stock analysis of small yellow croaker Larimichthys polyactis providing implications for stock conservation and management. Fisheries Research, 161: 86–92, DOI: https://doi.org/10.1016/j.fishres.2014.06.006.
Wu, P. Q., 1980. The morphological characters and seasonal changes in development of the oocytes of the small yellow croaker Pseudosciaena polycatis Bleeker. Acta Zoologica Sinica, 26(4): 337–346, DOI: https://doi.org/10.1111/j.1550-7480.1981.tb02793.x.
Wu, P. Q., 1981. Histological observations on the maturity of female gonad of the small yellow croaker Pseudosciaena polycatis Bleeker. Journal of Fisheries of China, 5(2): 161–169.
Wu, P. Q., 1982. Seasonal histological changes in the testis of small yellow croaker (Pseudosciaena polycatis Bleeker). Marine Sciences, 1982 (4):49.
Yang, F., Ye, H., Takeuchi, Y., Liu, F., and Xu, D. D., 2021. Characterization of the sex differentiation and gonadal development in small yellow croaker (Larimichthys polyactis) and its hybrid (L. polyactis ♀ × L. crocea ♂). Fish Physiology and Biochemistry, 47: 1467–1476, DOI: https://doi.org/10.1007/s10695-021-00975-0.
You, Y. L., and Lin, D. J., 1997. The ultrastructure of the spermatozoon of the teleosts, Pseudosciaena crocea (Richardson). Acta Zoological Sinica, 43(2): 119–126.
You, Y. L., Lin, D. J., and Chen, L. Y., 2001. Spermatogenesis of teleosts, Pseudosciaena crocea. Zoological Research, 22(6): 461–466, DOI: https://doi.org/10.3321/j.issn:0254-5853.2001.06.006.
Zhao, H. H., Liu, X. C., Lin, H. R., Liu, F. Y. Z., and Wang, Y. X., 2003. Ultrastructure of spermatozoa and effects of salinity, temperature and pH on spermatozoa motility in Epiniphelus coioides. Journal of Fishery Sciences of China, 10(4): 286–292, DOI: https://doi.org/10.3321/j.issn:1005-8737.2003.04.005.
Acknowledgements
We are thankful to all the members of the Fish Histology Laboratory at Ningbo University for valuable discussions. This study was supported by the NSFC-Zhejiang Joint Fund for the Integration of Industrialization and Informatization (No. U1809212), the Scientific and Technical Project of Zhejiang Province (Nos. 2021C02055, 2017C02013), the National Natural Science Foundation of China (No. 31272642), and Healthy Aquaculture, the K. C. Wong Magna Fund in Ningbo University and the Collaborative Innovation Center for Zhejiang Marine High-Efficiency.
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Zheng, X., Wang, J., Gao, X. et al. Testis Development and Ultrastructural Features During Spermatogenesis in Cultured Small Yellow Croaker, Larimichthys polyactis. J. Ocean Univ. China 22, 1412–1426 (2023). https://doi.org/10.1007/s11802-023-5529-1
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DOI: https://doi.org/10.1007/s11802-023-5529-1