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HERMAPHRODITISM IN GREY MULLET (MUGIL CEPHALUS) ALONG THE BULGARIAN BLACK SEA COAST: POTENTIAL CONNECTIONS TO ECOLOGICAL FACTORS
Abstract
Hermaphroditism in the flathead grey mullet (Mugil cephalus), manifested as intersex conditions, is linked to various environmental factors and anthropogenic pressures. Key contributors include exposure to endocrine-disrupting compounds (EDCs), heavy metals, and pollutants that disrupt hormonal regulation, leading to sexual development abnormalities. Research indicates that Mugil cephalus is particularly sensitive to EDCs in coastal and brackish ecosystems. Our findings reveal that 19% of male individuals from the Varna-Beloslav Lakes and the brackish waters at the mouths of the Kamchia, Ropotamo, Karaagach and Veleka Rivers exhibited intersex gonads correlated with elevated levels of organochlorine contaminants in their tissues. Laboratory experiments have shown that exposure to 17пїЅ-estradiol (E2) and ethinylestradiol (EE2) during sexual differentiation can induce feminisation and intersex conditions. In addition to EDCs, heavy metals pose significant genotoxic risks. A study in the Varna-Beloslav Lakes demonstrated that mullets exposed to high concentrations of metals such as CuпїЅ?, ZnпїЅ?, and PbпїЅ? exhibited increased frequencies of micronuclei and nuclear anomalies, indicating DNA damage. Climate change further impacts migratory behaviour and reproductive biology, mainly through rising sea surface temperatures. Our study along the Bulgarian Black Sea coast identified warming waters as a significant factor contributing to the decline in Mugil cephalus catches between 2010 and 2024. The combined effects of pollution and climate change synergistically enhance toxicity and increase contaminant sensitivity, amplifying reproductive risks for Mugil cephalus populations along the Bulgarian Black Sea coast.
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References34
Jobling, S., Nolan, M., Tyler, C.R., Brighty, G. and Sumpter, J.P., (1998). Widespread sexual disruption in wild fish. Environmental Science & Technology, 32(17), pp. 2498�2506. DOI: 10.1021/es980465j https://doi.org/10.1021/es9710870
Kidd, K.A., Blanchfield, P.J., Mills, K.H., Palace, V.P., Evans, R.E., Lazorchak, J.M. and Flick, R.W., (2007). Collapse of a fish population after exposure to a synthetic estrogen. Proceedings of the National Academy of Sciences, 104(21), pp. 8897�8901. DOI: 10.1073/pnas.0609568104
Sumpter, J.P. and Johnson, A.C., (2005). Lessons from endocrine disruption and their application to other issues concerning trace organics in the aquatic environment. Environmental Science & Technology, 39(12), pp. 4321�4332. DOI: 10.1021/es048963j https://doi.org/10.1021/es048504a
Hinck, J.E., Blazer, V.S., Schmitt, C.J., Papoulias, D.M. and Tillitt, D.E., (2006). Widespread occurrence of intersex in black basses (Micropterus spp.) from U.S. rivers, 1995�2004. Environmental Science & Technology, 40(21), pp. 7551�7558. DOI: 10.1021/es062066m
Blaber, S.J.M., (2000). Tropical estuarine fishes: Ecology, exploitation and conservation. Oxford: Blackwell Science, 384 pp. ISBN: 9780632051759 DOI: 10.1002/9780470694985
Guidetti, P., Magnelli, F. and Gramigni, E., (2004). Effects of coastal bottom trawling on the size structure of fish assemblages in the Southern Adriatic Sea (central Mediterranean). Aquatic Conservation: Marine and Freshwater Ecosystems, 14(6), pp. 575�589. DOI: 10.1002/aqc.636
Orlando, E.F., Kolok, A.S., Binzcik, G.A., Gates, J.L., Horton, M.K., Lambright, C.S., Gray Jr., L.E. and Soto, A.M., (2007). Endocrine-disrupting effects of cattle feedlot effluent on an aquatic sentinel species, the fathead minnow. Environmental Health Perspectives, 112(3), pp. 353�358. DOI: 10.1289/ehp.6575 https://doi.org/10.1289/ehp.6591
Blasco, J., Muse, J., Ruiz, F., Saenz, J. and Gonzalez de Canales, M., (2011). Intersex condition in Mugil cephalus from estuarine areas of the southwestern Spanish coast. Marine Environmental Research, 72(2), pp. 100�105. DOI: 10.1016/j. marenvres.2011.06.002
Zhou, Y., Chen, Y., Hu, Y., Yang, J. and Liu, L., (2014). Effects of 17�-estradiol and 17a-ethinylestradiol on gonadal development and reproduction in juvenile Mugil cephalus. Environmental Toxicology and Chemistry, 33(5), pp. 1157�1164. DOI: 10.1002/etc.2542
Bologa, A.S., Petranu, A., G�stescu, P., Dorogan, L., & Tiganov, G., (2000). Environmental state of the Romanian Black Sea coastal zone. Geo-Eco-Marina, 5�6, pp. 145�164.
Kideys, A.E., (2002). Fall and rise of the Black Sea ecosystem. Science, 297(5586), pp. 1482�1484. DOI: 10.1126/science.1073002
Topcuoglu, S., Erg�l, H.A., Esen, N. and Kut, D., (2002). Heavy metal and radionuclide levels in fish samples collected from the eastern Black Sea. Marine Pollution Bulletin, 44(10), pp. 1026�1030. DOI: 10.1016/S0025-326X(02)00135-4
Oros, A., T�r�k, Z., Navodaru, I. and Placinta, S., (2010). Mercury, cadmium and lead concentrations in fish from Danube Delta lakes. Environmental Engineering and Management Journal, 9(3), pp. 399�403. [ISSN: 1582-9596]
McDonough, C.J., Roumillat, W.A. and Wenner, C.A., (2003). Fecundity and spawning season of striped mullet (Mugil cephalus L.) in South Carolina estuaries. Fishery Bulletin, 101(4), pp. 822�834.
Brusl�, J., (1981). Sexuality and biology of reproduction of grey mullets. In: O.H. Oren (Ed.), Aquaculture of Grey Mullets, Cambridge University Press, Cambridge, pp. 99�154. ISBN: 9780521228473
Bahamonde, P.A., Munkittrick, K.R. and Martyniuk, C.J., (2013). Intersex in teleost fish: Are we distinguishing endocrine disruption from natural phenomena? General and Comparative Endocrinology, 192, pp. 25�35. DOI: 10.1016/j. ygcen.2013.04.005.ygcen.2013.04.005
Ferreira, M., Moradas-Ferreira, P. and Reis-Henriques, M.A., (2004). The effect of estrogenic compounds on the development of juvenile sea bass (Dicentrarchus labrax L.). Aquatic Toxicology, 68(4), pp. 385�398. DOI: 10.1016/j.aquatox.2004.04.004
Abdelhakim, N.T., El Sayed, A.M., Abdelaziz, M.E., Mekkawy, I.A. and Hegazy, R.E., (2020). Reproductive biology of the flathead grey mullet (Mugil cephalus, Linnaeus 1758) from Bardawil Lagoon, Egypt. The Egyptian Journal of Aquatic Research, 46(1), pp. 11�19. DOI: 10.1016/j.ejar.2019.10.001
Basusta, N., Demirel, N. and Akyol, O., (2021). Age, growth and reproduction of flathead grey mullet (Mugil cephalus) in the eastern Mediterranean Sea (Turkey). Journal of Applied Ichthyology, 37(1), pp. 34�41. DOI: 10.1111/jai.14137
Morozov, A.A., (1964). Biologicheskie osnovy promysla ryb Chernogo morya. Trudy VNIRO, 52, pp. 3�214. (In Russian)
Zhang, Y., Xu, H., Zhao, Y., Wang, X. and Lin, H., (2022). Gonadosomatic indices and seasonal reproductive dynamics in mullet species: Revisiting classical maturity models with updated biometric approaches. Fisheries Research, 253, 106347.DOI: 10.1016/j.fishres.2022.106347
Alonso-Fernandez, A., Dominguez-Petit, R., Saborido-Rey, F., (2021). Thermal sensitivity of reproductive timing in marine fish: insights from gonadal development and spawning phenology. Marine Environmental Research, 168, 105307. DOI: 10.1016/j.marenvres.2021.105307
Nikolopoulou, M., Tsiaras, K.P., Triantafyllou, G., Petihakis, G., (2020). Sea surface temperature trends in the eastern Mediterranean and the Black Sea: A 35-year satellite-based perspective. Remote Sensing, 12(10), 1597. DOI: 10.3390/rs12101597
Copernicus Marine Service, (2023). Sea surface temperature anomaly data for the Black Sea (1982�2023). Retrieved from: https://marine.copernicus.eu
Petric, M., Glamuzina, B., Ko�ul, V., Tutman, P., Skaramuca, B. and Franicevic, M., (2021). Reproductive dynamics of flathead grey mullet (Mugil cephalus) in the southeastern Adriatic Sea. Journal of Sea Research, 169, 102005. DOI: 10.1016/j.seares.2020.102005
Abdelhakim, N.T., El Sayed, A.M., Abdelaziz, M.E., Mekkawy, I.A. and Hegazy, R.E., (2020). Reproductive biology of the flathead grey mullet (Mugil cephalus, Linnaeus 1758) from Bardawil Lagoon, Egypt. The Egyptian Journal of Aquatic Research, 46(1), pp. 11�19. DOI: 10.1016/j.ejar.2019.10.001
Nikolopoulou, M., Tsiaras, K.P., Triantafyllou, G. and Petihakis, G., (2020). Sea surface temperature trends in the eastern Mediterranean and the Black Sea: A 35-year satellite-based perspective. Remote Sensing, 12(10), 1597. DOI: 10.3390/rs12101597
Miladinova, S., Stips, A., Garcia-Gorriz, E. and Macias, D., (2018). Black Sea thermohaline properties: Long-term trends and variations. Journal of Marine Systems, 180, pp. 17�28. DOI: 10.1016/j.jmarsys.2018.01.005
Alonso-Fernandez, A., Dominguez-Petit, R. and Saborido-Rey, F., (2021). Thermal sensitivity of reproductive timing in marine fish: Insights from gonadal development and spawning phenology. Marine Environmental Research, 168, 105307. DOI: 10.1016/j.marenvres.2021.105307
Dufour, S., Weltzien, F.A., Sebert, M.E., Le Belle, N. and Vidal, B., (2010). Seasonal control of reproduction in teleosts: lessons from the female European eel (Anguilla anguilla). Annals of the New York Academy of Sciences, 1200(1), pp. 105�115. DOI: 10.1111/j.1749-6632.2010.05556.x
Blazer, V.S., Iwanowicz, L.R., Iwanowicz, D.D., Smith, D.R., Young, J.A., Hedrick, J.D. and Reeser, S.J., (2007). Intersex (testicular oocytes) in smallmouth bass from the Potomac River and selected nearby drainages. Journal of Aquatic Animal Health, 19(4), pp. 242�253. DOI: 10.1577/H07-031.1
Barone, G., Gioia, I., Storelli, M.M. and Garofalo, R., (2020). Occurrence of endocrine-disrupting compounds in fish from Apulia (Southern Italy) and their potential risk. Environmental Science and Pollution Research, 27, pp. 34591�34601.DOI: 10.1007/s11356-020-09569-2
Jobling, S., Beresford, N., Nolan, M., Rodgers-Gray, T., Brighty, G.C., Sumpter, J.P. and Tyler, C.R., (2009). Altered sexual maturation and gamete production in wild roach (Rutilus rutilus) living in rivers that receive treated sewage effluents. Biology of Reproduction, 79(5), pp. 831�841. DOI: 10.1095/biolreprod.108.074674
Hinfray, N., Palluel, O., Piccini, B., Sanchez, W., A�t-A�ssa, S., Noury, P., Gomez, E. and Brion, F., (2010). Endocrine disruption in wild populations of chub (Leuciscus cephalus) in contaminated French streams. Science of The Total Environment, 408(9), pp. 2146�2154. DOI: 10.1016/j.scitotenv.2009.12.045 https://doi.org/10.1016/j.scitotenv.2010.01.003
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