Ultrasonography for sex determination of Lebranche mullet
DOI:
https://doi.org/10.20950/1678-2305/bip.2024.51.e902Keywords:
Gonads, Marine fish, Mugilidae, Reproduction, UltrasoundAbstract
Ultrasonography has been increasingly used in aquaculture breeding programs for non-invasive determination of sex and the gonad maturation stage in fish. For the first time, this image exam was performed on a mugilid (Lebranche mullet). Nineteen male and 12 female fish were submitted to this evaluation, which were selected because they were identified to be in the final gonad maturation stage, which was previously confirmed through spermiation by abdominal pressure and ovarian sampling biopsy (oocytes of 626 ± 12 μm), respectively. The ultrasound images were obtained after anesthesia, using a linear multifrequency probe at the frequency of 8 MHz in females and 10 MHz in males, which revealed significant differences in echogenicity between the gonads. In males, the testes presented a hypoechoic and homogeneous aspect, while in females the ovaries had a hyperechoic appearance and granular echotexture, compared to adjacent body structures. The scanning time for sexual identification and characterization of reproductive system structures in each fish was 2.58 ± 1.68 seconds for males and 2.40 ± 1.05 seconds for females, there was no significant difference (p > 0.05) in relation to sexing time. Thus, the identification of the sex of the Lebranche mullet (Mugil liza) through ultrasonography proved to be an effective, fast and non-invasive method when applied to fish with mature gonads during the species’ reproductive period.
References
Bahadir, K. (2023). Examination of studies on ultrasound applications on fish species and connection with aquatic mammals. Acta Scientific Veterinary Sciences, 5(7), 82-85. Retrieved from https://actascientific.com/ASVS/pdf/ASVS-05-0693.pdf
Barcaui, E. O., Carvalho, A. C. P., Piñeiro-Maceira, J., Barcaui, C. B., & Moraes, H. (2015). Estudo da anatomia cutânea com ultrassom de alta frequência (22 MHz) e sua correlação histológica. Radiologia Brasileira, 48(5), 324-329. https://doi.org/10.1590/0100-3984.2014.0028
Barroso, R. A., & Ueda, M. (2014). Ultrassonografia para identificação de sexo e estágios gonadais em espécies de peixes. Journal of Fish Biology, 85(5), 1479-1491.
Blythe, B., Helfrich, L. A., Beal, W. E., Bosworth, B., & Libey, G. S. (1994). Determination of sex and maturational status of striped bass (Morone saxatilis) using ultrasonic imaging. Aquaculture, 125(1-2), 195-184. https://doi.org/10.1016/0044-8486(94)90294-1
Bonar, S. A., Thomas, G. L., Pauley, G. B., & Martin, R. W. (1989). Management briefs: Use of ultrasonic images for rapid nonlethal determination of sex and maturity of Pacific herring. North American Journal of Fisheries Management, 9(3), 364-366.
https://doi.org/10.1577/1548-8675(1989)009<0364:MBUOUI>2.3.CO;2
Braz, R. S., Silva, I. O., Tesser, M. B., Sampaio, L. A., & Rodrigues, R. V. (2017). Benzocaine, MS-222, eugenol, and menthol as anesthetics for juvenile Mugil liza. Boletim do Instituto de Pesca, 43(4), 605-613. https://doi.org/10.20950/1678-2305.2017v43n4p605
Calixto, S. E., Sterzelecki, F. C., Musialak, A. L., Sugai, J. K., Castro, J. J. P., Pedrotti, F. S., Magnotti, C., Cipriano, F. S., Cerqueira, V. R. (2020). Effect of feeding frequency on growth performance, blood metabolites, proximate composition, and digestive enzymes of Lebranche mullet (Mugil liza) juveniles. Aquaculture Research, 51(3), 1162-1169. https://doi.org/10.1111/are.14466
Carvalho, C. F. (2014). Ultrassonografia em pequenos animais (2ª ed.). São Paulo: Roca.
Castro, J., Magnotti, C., Angelo, M., Sterzelecki, F., Pedrotti, F., Oliveira, M. F., Soligo, T., Fracalossi, D., & Cerqueira, V. R. (2019). Effect of ascorbic acid supplementation on zootechnical performance, haematological parameters, and sperm quality of lebranche mullet Mugil liza. Aquaculture Research, 50(11), 3267-3274. https://doi.org/10.1111/are.14284
Cerqueira, V. R., Carvalho, C. V. C., Sanches, E. G., Passini, G., Baloi, M., & Rodrigues, R. V. (2017). Manejo de reprodutores e controle da reprodução de peixes marinhos da costa brasileira. Revista Brasileira de Reprodução Animal, 41(1), 94-102. Retrieved from http://www.cbra.org.br/portal/downloads/publicacoes/rbra/v41/n1/p094-102%20(RB677).pdf
Colombier, S. B., Jacobs, L., Gesset, C., Elie, P., & Lambert, P. (2015). Ultrasonography as a non-invasive tool for sex determination and maturation monitoring in silver eels. Fisheries Research, 164, 50-58. https://doi.org/10.1016/j.fishres.2014.10.015
Crepaldi, D. V., Texeira, E. A., Faria, P. M. C., Ribeiro, L. P., Saturnino, H. M., Melo, D. C., Sousa, A. B., & Carvalho, D. C. A. (2006). Ultrassonografia na psicultura. Revista Brasileira de Reprodução Animal, 30(3-4), 174-181. Retrieved from http://www.cbra.org.br/pages/publicacoes/rbra/download/RB063%20Crepaldi%20(ultrasonografia)%20pag%20174-180.pdf
Doi, H., Murakami, S., Momota, K., Obata, H., & Sakai, H. (2024). Sex determination by ultrasonography prior to artificial breeding of the pufferfish Arothron manilensis (Tetraodontiformes, Tetraodontidae). Zoo Biology, 1(1-5), 287-291. https://doi.org/10.1002/zoo.21822
Du, H., Zhang, X., Leng, X., Zhang, S., Luo, J., Liu, Z., Qiao, X., Kynard, B., & Wei, Q. (2017). Gender and gonadal maturity stage identification of captive Chinese sturgeon, Acipenser sinensis, using ultrasound imagery and sex steroids. General and Comparative Endocrinology, 245, 36-43. https://doi.org/10.1016/j.ygcen.2016.08.004
Durand, J.-D., Shen, K.-N., Chen, W.-J., Jamandre, B.W., Blel, H., Diop, K., Nirchio, M., García de León, F.J., Whitfield, A.K., Chang, C.-W., & Borsa, P. (2012). Systematics of the grey mullets (Teleostei: Mugiliformes: Mugilidae): Molecular phylogenetic evidence challenges two centuries of morphologybased taxonomy. Molecular Phylogenetics and Evolution, 64(1), 73-92. https://doi.org/10.1016/j.ympev.2012.03.006
Frost, D. A., McAuley, W. C., Kluver, B., Wastel, M., Maynard, D., & Flagg, T. A. (2014). Methods and accuracy of sexing sockeye salmon using ultrasound for captive broodstock management. North American Journal of Aquaculture, 76,153-158. https://doi.org/10.1080/15222055.2014.886647
Golpour, A., Broquard, C., Milla, S., Dadras, H., Baloch, A., Saito, T., & Psenicka, M. (2021). Determination of annual reproductive cycle in male sterlet, Acipenser ruthenus using histology and ultrasound imaging. Fish Physiology and Biochemistry, 47(3), 703-711. https://doi.org/10.1007/s10695-020-00892-8
Jasaitiene, D., Valiukeviciene, S., Linkeviciute, G., Raisutis, R., Jasiuniene, E., Kazys, R. (2011). Principles of high-frequency ultrasonography for investigation of skin pathology. Journal of the European Academy of Dermatology and Venereology, 25(4), 375-382. https://doi.org/10.1111/j.1468-3083.2010.03837.x
Jennings, C. A., Sloss, B. L., Lasee, B. A., Burtle, G. J., & Moyer, G. R. (2012). Care, handling, and examination of sampled organisms and related tissues. In A. V. Zale, D. L. Parrish, & T. M. Sutton (Eds.), Fisheries techniques (3rd ed., pp.163-222). American Fisheries Society.
Jennings, C. A., Will, T. A., & Reinert, T. R. (2005). Efficacy of a high- and low-frequency ultrasonic probe for measuring ovary volume and estimating fecundity of striped bass Morone saxatilis in the Savannah River estuary. Fisheries Research, 76(3), 445-453. https://doi.org/10.1016/j.fishres.2005.07.016
Karlsen, O., & Holm, J.C. (1994). Ultrasonography, a noninvasive method for sex determination in cod (Gadus morhua). Journal of Fish Biology, 44(6), 965-971. https://doi.org/10.1111/j.1095-8649.1994.tb01268.x
Kerber, C. E., Azevedo Silva, H. K., Santos, P. A., & Sanches, E. G. (2012). Reproduction and larviculture of dusky grouper Epinephelus marginatus (Lowe 1834) in Brazil. Journal of Agricultural Science and Technology B, 2(2), 229-234. Retrieved from https://www.researchgate.net/publication/322666044_Reproduction_and_Larviculture_o f _ D u s k y _ G r o u p e r _ E p i n e p h e l u s _ m a rg i n a t u s _Lowe_1834_in_Brazil
Kohn, Y. Y., Lokman, P. M., Kilimnik, A., Symonds, J. E. (2013). Sex identification in captive hapuku (Polyprion oxygeneios) using ultrasound imagery and plasma 30 levels of vitellogenin and sex steroids. Aquaculture, 384-387, 87-93. https://doi.org/10.1016/j.aquaculture.2012.12.020
Kucharczyk, D., Żarski, D., Krejszeff, S., Nowosad, J., Biłas, M., Targonska, K., & Palinska-Zarska, K. (2016). Use of an ultrasound device to determine sex and to perform gonad biopsy in the European eel Anguilla anguilla. Brazilian Journal of Veterinary Research and Animal Science, 53(2), 199-206. https://doi.org/10.11606/issn.1678-4456.v53i2p199-206
Kujawa, R., Nowosad, J., Biegaj, M., Cejko, B., & Kucharczyk, D. (2019). Use of ultrasonography to determine sex in sexually immature European river lamprey Lampetra fluviatilis (L.). Animal Reproduction Science, 204, 95-100. https://doi.org/10.1016/j.anireprosci.2019.03.009
Loher, T., & Stephens, S. M. (2011). Use of veterinary ultrasound to identify sex and assess female maturity of Pacific halibut in nonspawning condition. North American Journal of Fisheries Management, 31(6), 1034-1042. https://doi.org/10.1080/02755947.2011.635240
Macri, F., Liotta, L., Bonfiglio, R., De Stefano, C., Ruscica, D., & Aiudi, G. (2013). Ultrasound measurement of reproductive organs in juvenile European sea bass Dicentrarchus labrax. Journal of Fish Biology, 83(5), 1439-1443. https://doi.org/10.1111/jfb.12228
Magnotti, C. C. F., Castro, J. D. J. P., Pedrotti, F. S., Sterzelecki, F. C., Sanches, E. G., & Cerqueira, V. R. (2018a). Shortterm storage of lebranche mullet Mugil liza (Valenciennes, 1836) semen in natura and diluted with CF-HBSS. Acta Scientiarum. Animal Sciences, 40(1), 39563. https://doi.org/10.4025/actascianimsci.v40i1.39563
Magnotti, C. C. F., Cipriano, F. S., Pedrotti, F. S., & Cerqueira, V. R. (2020). Advances in reproduction of the lebranche mullet Mugil liza: Maturation and spawning of F1 breeders in captivity. Boletim do Instituto de Pesca, 46(3), e586. https://doi.org/10.20950/1678-2305.2020.46.3.586
Magnotti, C. C. F., Figueroa, E., Farias, J. G., Merino, O., Valdebenito, I., Oliveira, R. P. S., & Cerqueira, V. (2018b). Sperm characteristics of wild and captive lebranche mullet Mugil liza (Valenciennes, 1836), subjected to sperm activation in different pH and salinity conditions. Animal Reproduction Science, 192(1), 164-170. https://doi.org/10.1016/j.anireprosci.2018.03.004
Martin-Robichaud, D. J., & Rommens, M. (2001). Assessment of sex and evaluation of ovarian maturation of fish using ultrasonography. Aquaculture Research, 32, 113-120. https://doi.org/10.1046/j.1365-2109.2001.00538.x
Masoudifard, M., Vajhi, A., Moghim, M., Nazari, R. M., Naghavi, A. R., & Sohrabnejad, M. (2011). High validity sex determination of three-year-old cultured beluga sturgeon (Huso huso) using ultrasonography. Journal of Applied Ichthyology, 27, 643-647. https://doi.org/10.1111/j.1439-0426.2011.01726.x
Masoudifard, M., Vajhi, A., Mohammadshahali, S., Zehtabvar, O., Moghim, M., & Mirhashemi, S. A. (2023). Ultrasonographic sex determination of the flathead grey mullet (Mugil cephalus). Veterinary Medicine and Science, 9(2), 802-809. https://doi.org/10.1002/vms3.1066
Matsubara, T. K., Yamanome, W. T., & Kayaba, T. (1999). Application of ultrasonography to non-invasive sexing based on the sexual dimorphism in gonads of immature barfin flounder Verasper moseri. Fisheries Science, 65(2), 244-247. https://doi.org/10.2331/fishsci.65.244
Mattson, N. S. (1991). A new method to determine sex and gonad size in live fishes by using ultrasonography. Journal of Fish Biology, 39(5), 673-677. https://doi.org/10.1111/j.1095-8649.1991.tb04397.x
McDowall, R. M. (2007). On amphidromy, a distinct form of diadromy in aquatic organisms. Fish and Fisheries, 8(1), 1-13. https://doi.org/10.1111/j.1467-2979.2007.00232.x
McEvoy, F. J., Tomkiewicz, J., Støttrup, J. G., Overton, J. L., McEvoy, C., & Svalastoga, E. (2009). Determination of fish gender using fractal analysis of ultrasound images. Veterinary Radiology and Ultrasound, 50(9), 519-524. https://doi.org/10.1111/j.1740-8261.2009.01568.x
Memis, D., Yamaner, G., Tosun, D. D., Eryalcin, K. M., Chebanov, M., & Galich, E. (2016). Determination of sex and gonad maturity in sturgeon (Acipenser gueldenstaedtii) using ultrasound technique. Journal of Applied Aquaculture, 28(3), 252-259. https://doi.org/10.1080/10454438.2016.1174181
Menezes, N. A. (1983). Guia prático para o reconhecimento e identificação de tainhas e paratis (Pisces, Mugilidae) do litoral brasileiro. Revista Brasileira de Zoologia, 2(1), 1-12. https://doi.org/10.1590/S0101-81751983000100001
Menezes, N. A., & Figueiredo, J. L. (1985). Manual de peixes marinhos do Sudeste do Brasil. Museu de Zoologia USP, 306(4). Retrieved from https://www.researchgate.net/publication/285464283_Manual_de_peixes_marinhos_do_Sudeste_do_Brasil_II_Museu_Zoololgia_da_USP_Sao_Paulo
Menezes, N. A., Nirchio, M., Oliveira, C. D., & Siccharamirez, R. (2015). Taxonomic review of the species of Mugil (Teleostei: Perciformes: Mugilidae) from the Atlantic South Caribbean and South America, with integration of morphological, cytogenetic and molecular data. Zootaxa, 3918(1), 1-38. https://doi.org/10.11646/zootaxa.3918.1.1
Mlingi, F. T., Puvanendran, V., Burgerhout, E., Tveiten, H., Tomkiewicz, J., Kjørsvik, E., & Mommens, M. (2023). Ultrasonic imaging as a means of monitoring gonadal development in lumpfish (Cyclopterus lumpus). Physiological Reports, 11(18), 1-12. https://doi.org/10.14814/phy2.15811
Moghim, M., Vajhi, A. R., Veshkini, A., & Masoudifard, M. (2002). Determination of sex and maturity in Acipenser stellatus by using ultrasonography. Journal of Applied Ichthyology, 18(4-6), 325-328. https://doi.org/10.1046/j.1439-0426.2002.00423.x
Müller, A. V., McEvoy, F. J., Tomkiewicz, J., Politis, S. N., & Amigo, J. M. (2015). Ultrasonographic predictors of response of European eels (Anguilla anguilla) to hormonal treatment for induction of ovarian development. American Journal of Veterinary Research, 77(5), 478-486. https://doi.org/10.2460/ajvr.77.5.478
Næve, I., Mommens, M., Arukwe, A., & Kjørsvik, E. (2018). Ultrasound as a noninvasive tool for monitoring reproductive physiology in female Atlantic salmon (Salmo salar). Physiological Reports, 6(9), e13640. https://doi.org/10.14814/phy2.13640
Novelo, N. D., & Tiersch, T. R. (2012). A review of the use of ultrasonography in fish reproduction. North American Journal of Aquaculture, 74(2), 169-181. https://doi.org/10.1080/15222055.2012.672370
Papaléo, R. M., & de Souza, D. S. (2019). Ultrassonografia: Princípios físicos e controle da qualidade. Revista Brasileira De Física Médica, 13(1), 14-23. https://doi.org/10.29384/rbfm.2019.v13.n1.p14-23
Peixoto, G., Lira, R., Alves, N., & Silva, A. (2010). Bases físicas da formação da imagem ultrassonográfica. Acta Veterinaria Brasilica, 4(1), 15-24. Retrieved from https://periodicos.ufersa.edu.br/acta/article/view/1538/4503
Penninck, D., & d’Anjou, M. (2017). Conceptos físicos prácticos y artefactos. In Atlas de ecografía en pequeños animals (2ª ed.). Wiley-Blackwell.
Preston, C., & Shaw, A. (2001). Recommended ultrasound field safety classification for medical diagnostic devices (pp. 1-18). National Physics Laboratory. Retrieved from https://eprintspublications.npl.co.uk/2113/
Sampaio, L. A., Robaldo, R. B., & Bianchini, A. (2008). Hormone induced ovulation, natural spawning and larviculture of Brazilian flounder Paralichthys orbignyanus (Valenciennes, 1839). Aquaculture Research, 39(7), 712- 717. https://doi.org/10.1111/j.1365-2109.2008.01923.x
Siccha-Ramirez, R., Menezes, N. A., Nirchio, M., Foresti, F. & Oliveira, C. (2014). Molecular identification of mullet species of the Atlantic South Caribbean and South America and the phylogeographic analysis of Mugil liza. Reviews in Fisheries Science & Aquaculture, 22(1), 86-96. https://doi.org/10.1080/10641262.2013.833583
Vajhi, A., Veshkini, A., Masoudifard, M., Moghim, M., & Molazem, M. (2013). Ultrasonographic findings of ovary and testis in adult Acipenser persicus during artificial propagation (stage V of maturity). Iranian Journal of Veterinary Surgery, 8(1), 17-22. https://doi.org/20.1001.1.20083033.2013.08.1.2.8
Whiteman, E. A., Jennings, C. A., & Nemeth, R. S. (2005). Sex structure and potential female fecundity in a Epinephelus guttatus spawning aggregation: Applying ultrasonic imaging. Journal of Fish Biology, 66(4), 983-995. https://doi.org/10.1111/j.0022-1112.2005.00653.x
Downloads
Published
Issue
Section
License
Copyright (c) 2025 Ingrith Mazuhy Santarosa, Maria Alcina de Castro, Marina Cesconeto dos Santos, Liseth Carolina Perenguez Riofrio, Aline Brum, Caio Magnotti
This work is licensed under a Creative Commons Attribution 4.0 International License.
