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Effects of exposure to the UV-filter 4-MBC during Solea senegalensis metamorphosis

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Abstract

Many personal care products integrate UV-filters, such as 4-methylbenzylidene camphor (4-MBC), a compound frequently detected in aquatic habitats, including coastal areas. However, the potential effects of 4-MBC to saltwater species have been poorly studied. Therefore, the main objective of this work is to study the effects of 4-MBC exposure on Solea senegalensis during metamorphosis, a sensitive life stage of this flatfish. To achieve this, fish were exposed to 4-MBC (0.2–2.0 mg L-1) for 48 h at the beginning of metamorphosis (13 days after hatching, dah). After this period, the fish were transferred to a clean medium. They were fed and maintained until more than 80% of individuals in the control group completed the metamorphosis (24 dah). Mortality, malformations, and metamorphic progression were studied daily. Growth, behavior, and biochemical markers of neurotransmission (acetylcholinesterase, AChE), oxidative stress (catalase, CAT; lipid peroxidation, LPO), detoxification (glutathione S-transferase, GST), and anaerobic metabolism (lactate dehydrogenase, LDH) were also determined at the end of the experiment. An acceleration of metamorphosis progression was observed during and 2 days after the 4-MBC exposure in all concentrations tested. In addition, reduced length, inhibition of CAT activity, and induction of oxidative damage were observed (lowest observed effect concentration, LOEC = 0.928 mg L−1 4-MBC for length, CAT, and LPO). Short-term exposure to 4-MBC at the onset of metamorphosis affected S. senegalensis at several levels of organization, even after 9 days in a clean medium, including growth and metamorphic progression, suggesting possible long-term adverse effects in this species.

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All data generated or analyzed during this study are included in this published article [and its supplementary information files].

References

  • Agbohessi TP, Toko II, N’tcha I, Geay F, Mandiki SNM, Kestemont P (2014) Exposure to agricultural pesticides impairs growth, feed utilization and energy budget in African Catfish Clarias gariepinus (Burchell, 1822) fingerlings. Int Aquat Res 6(4):229–243

  • Ahmed F, Ghalib RM, Sasikala P, Ahmed KK (2013) Cholinesterase inhibitors from botanicals. Pharmacogn Rev 7(14):121–130. https://doi.org/10.4103/0973-7847.120511

    Article  CAS  Google Scholar 

  • Almeida JR, Gravato C, Guilhermino L (2015) Effects of temperature in juvenile Seabass (Dicentrarchus labrax L.) biomarker responses and behaviour: implications for environmental monitoring. Estuar Coasts 38:45–55. https://doi.org/10.1007/s12237-014-9792-7

    Article  CAS  Google Scholar 

  • Anacleto P, Figueiredo C, Baptista M, Maulvault AL, Camacho C, Pousão-Ferreira P, Valente LMP, Marques A, Rosa R (2018) Fish energy budget under ocean warming and flame retardant exposure. Environ Res 164:186–196. https://doi.org/10.1016/j.envres.2018.02.023

    Article  CAS  Google Scholar 

  • Anguis V, Cañavate JP (2005) Spawning of captive Senegal sole (Solea senegalensis) under a naturally fluctuating temperature regime. Aquaculture 243(1-4):133–145. https://doi.org/10.1016/j.aquaculture.2004.09.026

    Article  Google Scholar 

  • Araújo MJ, Rocha RJM, Soares AMVM, Chisvert A, Monteiro MS (2018) Effects of UV filter 4-methylbenzylidene camphor during early development of Solea senegalensis Kaup, 1858. Sci Total Environ 628-629:1395–1404. https://doi.org/10.1016/j.scitotenv.2018.02.112

    Article  CAS  Google Scholar 

  • Araújo MJ, Quintaneiro C, Soares AMVM, Monteiro MS (2019) Effects of triclosan on early development of Solea senegalensis: from biochemical to individual level. Chemosphere 235:885–899

    Article  Google Scholar 

  • Araújo MJ, Quintaneiro C, Soares AMVM, Monteiro MS (2020) Effects of ultraviolet radiation to Solea senegalensis during early development. Sci Total Environ 764:142899. https://doi.org/10.1016/j.scitotenv.2020.142899

    Article  CAS  Google Scholar 

  • Arnholt A.T., 2016. Passion Driven Statistics. Available at https://alanarnholt.github.io.

  • Balmer M, Buser HR, Muller M, Poiger T (2005) Occurrence of some organic UV filters in wastewater, in surface waters, and in fish from Swiss lakes. Environ Sci Technol 39:953–962

    Article  CAS  Google Scholar 

  • Bayarri MJ, Muñoz-Cueto JA, López-Olmeda JF, Vera LM, Rol de Lama MA, Madrid JA, Sánchez-Vázquez FJ (2004) Daily locomotor activity and melatonin rhythms in Senegal sole (Solea senegalensis). Physiol Behav 81(4):577–583

    Article  CAS  Google Scholar 

  • Bird RP, Draper HH (1984) Comparative studies on different methods of malonaldehyde determination. Methods Enzymol 105:299–305

    Article  CAS  Google Scholar 

  • Blanco-Vives B, Aliaga-Guerrero M, Cañavate JP, García-Mateos G, Martín-Robles AJ, Herrera-Pérez P, Muñoz-Cueto JA, Sánchez-Vázquez FJ (2012) Metamorphosis induces a light-dependent switch in Senegalese sole (Solea senegalensis) from diurnal to nocturnal behavior. J Biol Rhythm 27:135–144. https://doi.org/10.1177/0748730411435303

    Article  CAS  Google Scholar 

  • Blanco-Vives B, Aliaga-Guerrero M, Cañavate JP, Muñoz-Cueto JA, Sánchez-Vázquez FJ (2011) Does lighting manipulation during incubation affect hatching rhythms and early development of sole? Chronobiol Int 28(4):300–306. https://doi.org/10.3109/07420528.2011.560316

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Brown MR, Blackburn SI (2013) Live microalgae as feeds in aquaculture hatcheries. In: Advances in Aquaculture Hatchery Technology (Editors: Geoff Allan and Gavin Burnell). Woodhead Publishing Series in Food Science, Technology and Nutrition. 117-156, 157e-158e. https://doi.org/10.1533/9780857097460.1.117.

  • Buser HR, Balmer ME, Schmid P, Kohler M (2006) Occurrence of UV filters 4-Methylbenzylidene camphor and octocrylene in fish from various Swiss rivers with inputs from wastewater treatment plants. Environ Sci Technol 40(5):1427–1431

    Article  CAS  Google Scholar 

  • Campos C, Castanheira MF, Engrola S, Valente LM, Fernandes JM, Conceição LE (2013) Rearing temperature affects Senegalese sole (Solea senegalensis) larvae protein metabolic capacity. Fish Physiol Biochem 39(6):1485–1496. https://doi.org/10.1007/s10695-013-9802-x

    Article  CAS  Google Scholar 

  • Campos D, Gravato C, Fedorova G, Burkina V, Soares AMVM, Pestana JLT (2017a) Ecotoxicity of two organic UV-filters to the freshwater caddisfly Sericostoma vittatum. Environ Pollut 228:370–377. https://doi.org/10.1016/j.envpol.2017.05.021

    Article  CAS  Google Scholar 

  • Campos D, Gravato C, Quintaneiro C, Golovko O, Žlábek V, Soares AMVM, Pestana JLT (2017b) Toxicity of organic UV-filters to the aquatic midge Chironomus riparius. Ecotoxicol Environ Saf 143:210–216. https://doi.org/10.1016/j.ecoenv.2017.05.005

    Article  CAS  Google Scholar 

  • Capela D, Vila M, Llompart M, Dagnac T, García-Jares C, Alves A, Homem V (2019) Footprints in the sand – Assessing the seasonal trends of volatile methylsiloxanes and UV-filters. Mar Pollut Bull 140:9–16. https://doi.org/10.1016/j.marpolbul.2019.01.021

    Article  CAS  Google Scholar 

  • Chisvert A, Salvador A (2018) UV filters in sunscreens and other cosmetics: regulatory aspects and analytical methods. In: Salvador A, Chisvert A (eds) Analysis of Cosmetics Products, second edn. Elsevier, Amsterdam, pp 85–106

  • Clairborne A (1985) Catalase activity. In: Greenwald RA (ed) CRC Handbook of Methods in Oxygen Radical Research. CRC Press, Boca Raton, FL, pp 283–284

    Google Scholar 

  • Crofton KM, Paul KB, Devito MJ, Hedge JM (2007) Short-term in vivo exposure to the water contaminant triclosan: Evidence for disruption of thyroxine. Environ Toxicol Pharmacol 24(2):194–197. https://doi.org/10.1016/j.etap.2007.04.008

    Article  CAS  Google Scholar 

  • Crofton KM (2008) Thyroid disrupting chemicals: mechanisms and mixtures. Int J Androl 31:209–223. https://doi.org/10.1111/j.1365-2605.2007.00857.x

    Article  CAS  Google Scholar 

  • Diamantino T, Almeida E, Soares AMVM, Guilhermino L (2001) Lactate dehydrogenase activity as an effect criterion in toxicity tests with Daphia magna Straus. Chemosphere 45(4-5):553–560. https://doi.org/10.1016/S0045-6535(01)00029-7

    Article  CAS  Google Scholar 

  • Dinis MT (1986) Quatre soleidae de l'estuaire du Tage. Reproduction et croissance. Essai d'elevage de Solea senegalensis Kaup. Université de Bretagne Occidentale. Brest. Ph.D. dissertation.

  • Dong Y, Zhang X, Tian H, Li X, Wang W, Ru S (2017) Effects of polychlorinated biphenyls on metamorphosis of a marine fish Japanese flounder (Paralichthys olivaceus) in relation to thyroid disruption. Mar Pollut Bull 119(1):325–331. https://doi.org/10.1016/j.marpolbul.2017.04.033

    Article  CAS  Google Scholar 

  • Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):88–95

    Article  CAS  Google Scholar 

  • Fernández-Díaz C, Kopecka J, Cañavate JP, Sarasquete C, Solé M (2006) Variations on development and stress defences in Solea senegalensis larvae fed on live and microencapsulated diets. Aquaculture 251:573–584

    Article  Google Scholar 

  • Fernández-Díaz D, Yúfera M, Cañavate JP, Moyano FJ, Alarcón FJ, Díaz M (2001) Growth and physiological changes during metamorphosis of Senegal sole reared in the laboratory. J Fish Biol 58(4):1086–1097. https://doi.org/10.1111/j.1095-8649.2001.tb00557.x

    Article  Google Scholar 

  • Frasco MF, Guilhermino L (2002) Effects of dimethoate and beta-naphthoflavone on selected biomarkers of Poecilia reticulata. Fish Physiol Biochem 26(2):149–156

    Article  CAS  Google Scholar 

  • Gago-Ferrero P, Díaz-Cruz MS, Barceló D (2012) An overview of UV-absorbing compounds (organic UV filters) in aquatic biota. Anal Bioanal Chem 404:2597–2610. https://doi.org/10.1007/s00216-012-6067-7

    Article  CAS  Google Scholar 

  • Gao L, Yuan T, Zhou C, Cheng P, Bai Q, Ao J, Wang W, Zhang H (2013) Effects of four commonly used UV filters on the growth, cell viability and oxidative stress responses of the Tetrahymena thermophila. Chemosphere 93(10):2507–2513. https://doi.org/10.1016/j.chemosphere.2013.09.04

    Article  CAS  Google Scholar 

  • García-de-la-Parra L.M., Bautista-Covarrubias J.C, Rivera-de la Rosa N., Betancourt-Lozano M, Guilhermino L., 2006. Effects of methamidophos on acetylcholinesterase activity, behavior, and feeding rate of the white shrimp (Litopenaeus vannamei). Ecotoxicol Environ Saf, 65(3): 372-380.

  • Gotthardt I, Schmutzler C, Kirschmeyer P, Wuttke W, Jarry H, Köhrle J (2007) 4-methylbenzylidene-camphor (4MBC) causes effects comparable to primary hypothyroidism. Exp Clin Endocrinol Diabetes 115:P02_014. https://doi.org/10.1055/s-2007-972421

    Article  Google Scholar 

  • Guilhermino L, Lopes MC, Carvalho AP, Soares AMVM (1996) Inhibition of acetylcholinesterase activity as elect criterion in acute tests with juvenile Daphnia magna. Chemosphere 32:727–738

    Article  CAS  Google Scholar 

  • Güngördü A, Uçkun M, Yoloğlu E (2016) Integrated assessment of biochemical markers in premetamorphic tadpoles of three amphibian species exposed to glyphosate- and methidathion-based pesticides in single and combination forms. Chemosphere 144:2024–2035. https://doi.org/10.1016/j.chemosphere.2015.10.125

    Article  CAS  Google Scholar 

  • Habig WH, Jakoby WB (1981) Assays for differentiation of glutathione S-transferases. Methods Enzymol 77:398–405

    Article  CAS  Google Scholar 

  • Henriques JF, Almeida AR, Andrade T, Koba O, Golovko O, Soares AMVM, Oliveira M, Domingues I (2016) Effects of the lipid regulator drug gemfibrozil: A toxicological and behavioral perspective. Aquat Toxicol 170:355–364. https://doi.org/10.1016/j.aquatox.2015.09.017

    Article  CAS  Google Scholar 

  • Imsland AK, Foss A, Conceição LEC, Dinis MT, Delbare D, Schram E, Kamstra A, Rema P, White P (2003) A review of the culture potential of Solea solea and S. senegalensis. Rev Fish Biol Fish 13:379–407

    Article  Google Scholar 

  • Kashiwagi A, Hanada H, Yabuki M, Kanno T, Ishisaka R, Sasaki J, Inoue M, Utsumi K (1999) Thyroxine enhancement and the role of reactive oxygen species in tadpole tail apoptosis. Free Radic Biol Med 26(7-8):1001–1009

    Article  CAS  Google Scholar 

  • Kieffer JD (2000) Limits to exhaustive exercise in fish. Comp Biochem Physiol A Mol Integr Physiol 126(2):161–179

    Article  CAS  Google Scholar 

  • Klaren PHM, Wunderink YS, Yúfera M, Mancera JM, Flik G (2008) The thyroid gland and thyroid hormones in Senegalese sole (Solea senegalensis) during early development and metamorphosis. Gen Comp Endocrinol 155:686–694

    Article  CAS  Google Scholar 

  • Krause M, Klit A, Blomberg-Jensen M, Søeborg T, Frederiksen H, Schlumpf M, Lichtensteiger W, Skakkebaek NE, Drzewiecki KT (2012) Sunscreens: Are they beneficial for health? An overview of endocrine disrupting properties of UV-filters. Int J Androl 35(3):424–436. https://doi.org/10.1111/j.1365-2605.2012.01280.x

    Article  CAS  Google Scholar 

  • Langford KH, Thomas KD (2008) Inputs of chemicals from recreational activities into the Norwegian coastal zone. J Environ Monit 10:894–898

    Article  CAS  Google Scholar 

  • Li VW, Tsui MP, Chen X, Hui MN, Jin L, Lam RH, Yu RM, Murphy MB, Cheng J, Lam PK, Cheng SH (2016) Effects of 4-methylbenzylidene camphor (4MBC) on neuronal and muscular development in zebrafish (Danio rerio) embryos. Environ Sci Pollut Res 23(9):8275–8285. https://doi.org/10.1007/s11356-016-6180-9

    Article  CAS  Google Scholar 

  • Li W, Ma Y, Guo C, Hu W, Liu K, Wang Y, Zhu T (2007) Occurrence and behaviour of four of the most used sunscreen UV filters in a wastewater reclamation plant. Water Res 41(15):3506–3512. https://doi.org/10.1016/j.watres.2007.05.039

    Article  CAS  Google Scholar 

  • Lowe N (2006) An overview of ultraviolet radiation, sunscreens, and photo-induced dermatoses. Dermatol Clin 24(1):9–17. https://doi.org/10.1016/j.det.2005.08.001

    Article  CAS  Google Scholar 

  • Luthe G, Jacobus JA, Robertson LW (2008) Receptor interactions by polybrominated diphenyl ethers versus polychlorinated biphenyls: a theoretical Structure-activity assessment. Environ Toxicol Pharmacol 25(2):202–210. https://doi.org/10.1016/j.etap.2007.10.017

    Article  CAS  Google Scholar 

  • Mach M, Grubbs RD, Price WA, Paton SJ, Lucot JB (2004) Behavioral changes after acetylcholinesterase inhibition with physostigmine in mice. Pharmacol Biochem Behav 79(3):533–540

    Article  CAS  Google Scholar 

  • Martins D, Monteiro MS, Soares AMVM, Quintaneiro C (2017) Effects of 4-MBC and triclosan in embryos of the frog Pelophylax perezi. Chemosphere 178:325–332

    Article  CAS  Google Scholar 

  • McKenzie DJ (2011) Energy utilisation: the energetics of swimming. In: Farrell AP, Cech JJ, Richards JG, Stevens ED (eds) Encyclopedia of fish physiology, from genome to environment. Elsevier, San Diego, California

    Google Scholar 

  • Menon J, Rozman R (2007) Oxidative stress, tissue remodeling and regression during amphibian metamorphosis. Comp Biochem Physiol C Toxicol Pharmacol 145(4):625–631

  • Morais S, Aragão C, Cabrita E, Conceição LEC, Constenla M, Costas B, Dias J, Duncan N, Engrola S, Estevez A, Gisbert E, Mañanós E, Valente LMP, Yúfera M, Dinis MT (2016) New developments and biological insights into the farming of Solea senegalensis reinforcing its aquaculture potential. Rev Aquac 8:227–263. https://doi.org/10.1111/raq.12091

    Article  Google Scholar 

  • Okada N., Tanaka M., Tagawa M., (2003) Bone development during metamorphosis of the Japanese flounder (Paralichthys olivaceus): differential responses to thyroid hormone. In The Big Fish Bang. Proceedings of the 26th Annual Larval Fish Conference (Browman HI and Skiftesvik AB, eds). Bergen: Institute of Marine Research, 11 pp.

  • Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13(2):57–149

    Article  Google Scholar 

  • Ozáez I, Martínez-Guitarte JL, Morcillo G (2013) Effects of in Vivo Exposure to UV Filters (4-MBC, OMC, BP-3, 4-HB, OC, OD-PABA) on Endocrine Signaling Genes in the Insect Chironomus Riparius. Sci Total Environ 456-457:120–126. https://doi.org/10.1016/j.scitotenv.2013.03.081

    Article  CAS  Google Scholar 

  • Pavlaki M, Araújo M, Cardoso D, Silva AR, Cruz A, Mendo S, Soares AMVM, Calado R, Loureiro S (2016) Ecotoxicity and genotoxicity of cadmium in different marine trophic levels. Environ Pollut 215:203–212

    Article  CAS  Google Scholar 

  • Pimentel M, Faleiro F, Diniz M, Machado J, Pousão-Ferreira P, Peck M, Pörtner H, Rosa R (2015) Oxidative stress and digestive enzyme activity of flatfish larvae in a changing ocean. PLoS One 10(7):e0134082

    Article  Google Scholar 

  • Power DM, Einarsdottir I, Pittman K, Sweeney G, Hildahl J, Campinho MA, Silva N, Saele O, Galay-Burgos M, Smaradottir H, Björnsson BT (2008) The molecular and endocrine basis of flatfish metamorphosis. Rev Fish Sci 16(1):93–109

    Google Scholar 

  • Quintaneiro C, Teixeira B, Benedé JL, Chisvert A, Soares AMVM, Monteiro MS (2019) Toxicity effects of the organic UV-filter 4-Methylbenzylidene camphor in zebrafish embryos. Chemosphere 218:273–281. https://doi.org/10.1016/j.chemosphere.2018.11.096

    Article  CAS  Google Scholar 

  • Rabasa C, Dickson SL (2016) Impact of stress on metabolism and energy balance. Curr Opin Behav Sci 6:71–77. https://doi.org/10.1016/j.cobeha.2016.01.011

    Article  Google Scholar 

  • Rao JV, Begum G, Pallela R, Usman PK, Rao RN (2005) Changes in behavior and brain acetylcholinesterase activity in mosquito fish, Gambusia affinis in response to the sub-lethal exposure to chlorpyrifos. Int J Environ Res Public Health 2(3-4):478–483

    Article  CAS  Google Scholar 

  • Rudneva I, Kuzminova N, Skuratovskaya E (2010) Glutathione-S-Transferase Activity in tissues of Black Sea fish species. Asian J Exp Biol Sci 1(1):141–150

  • Sánchez-Rodríguez A, Sanz MR, Betancort J (2015) Occurrence of eight UV filters in beaches of Gran Canaria (Canary Islands). An approach to environmental risk assessment. Chemosphere 131:85–90

    Article  Google Scholar 

  • Sarasquete C., Gisbert E., Ortiz-Delgado J.B. (2019) Embryonic and Larval Ontogeny of the Senegalese Sole, Solea senegalensis: Normal Patterns and Pathological Alterations. In: The Biology of Sole (Muñoz-Cueto J.,A., Sánchez E., L., M., Sánchez-Vázquez F.J., (Eds) CRC Press. 448 pp. ISBN 9781498727839.

  • Schmutzler C, Gotthardt I, Hofmann PJ, Radovic B, Kovacs G, Stemmler L, Nobis L, Bacinski A, Mentrup B, Ambrugger P, Grüters A, Malendowicz LK, Christoffel J, Jarry H, Seidlovà-Wuttke D, Wuttke W, Köhrle J (2007) Endocrine disruptors and the thyroid gland — a combined in vitro and in vivo analysis of potential new biomarkers. Environ Health Perspect 115(Suppl 1):77–83. https://doi.org/10.1289/ehp.9369

    Article  Google Scholar 

  • Schreiber AM (2013) Flatfish: An Asymmetric Perspective on Metamorphosis. Curr Top Dev Biol 103:167–194. https://doi.org/10.1016/B978-0-12-385979-2.00006-X

    Article  CAS  Google Scholar 

  • Scott GR, Sloman KA (2004) The effects of environmental pollutants on complex fish behaviour: integrating behavioural and physiological indicators of toxicity. Aquat Toxicol 68(4):369–392. https://doi.org/10.1016/j.aquatox.2004.03.016

    Article  CAS  Google Scholar 

  • Sharma M (2019) Behavioural responses in effect to chemical stress in fish: A review. Int J Fish Aquat Stud 7(1):01–05

  • Shoji J, Toshito S, Mizuno K, Kamimura Y, Hori M, Hirakawa K (2011) Possible effects of global warming on fish recruitment: shifts in spawning season and latitudinal distribution can alter growth of fish early life stages through changes in day length. ICES J Mar Sci 68:1165–1169

    Article  Google Scholar 

  • Sloman KA, McNeil PL (2012) Using physiology and behavior to understand the responses of fish early life stages to toxicants. J Fish Biol 81(7):2175–2198

    Article  CAS  Google Scholar 

  • Sowers AD, Klaine SJ (2008) The effects of triclosan on the development of Rana palustris. Proceedings of the 2008 South Carolina Water Resources Conference, October 14-15, 2008, USA.

  • Sun M, Wei F, Li H, Xu J, Chen X, Gong X, Tian Y, Chen S, Bao B (2015) Distortion of frontal bones results from cell apoptosis by the mechanical force from the up-migrating eye during metamorphosis in Paralichthys olivaceus. Mech Dev 136:87–98

    Article  CAS  Google Scholar 

  • Tata JR (1994) Hormonal regulation of programmed cell death during amphibian metamorphosis. Biochem Cell Biol 72(11-12):581–588

    Article  CAS  Google Scholar 

  • Torres JJ, Grigsby MD, Clarke ME (2012) Aerobic and anaerobic metabolism in oxygen minimum layer fishes: the role of alcohol dehydrogenase. J Exp Biol 215:1905–1914. https://doi.org/10.1242/jeb.060236

    Article  CAS  Google Scholar 

  • Torres T, Cunha I, Martins R, Santos MM (2016) Screening the toxicity of selected personal care products using embryo bioassays: 4-MBC, propylparaben and triclocarban. Int J Mol Sci 17(10):1762

    Article  Google Scholar 

  • Tovar-Sánchez A, Sánchez-Quiles D, Basterretxea G, Benedé JL, Chisvert A, Salvador A, Moreno I, Blasco J (2013) Sunscreen products as emerging pollutants to coastal waters. PLoS One 8(6):e65451. https://doi.org/10.1371/journal.pone.0065451

    Article  CAS  Google Scholar 

  • United States Environmental Protection Agency (USEPA) (2012) 40 CFR Part 423 - 126 Priority Pollutants. Appendix A. United States Environmental Protection Agency. Washington, USA.

  • Vassault A (1983) Methods of enzymatic analysis. Academic Press, New York, pp 118–126

    Google Scholar 

  • Veldhoen N, Skirrow RC, Osachoff H, Wigmore H, Clapson DJ, Gunderson MP, Van Aggelen G, Helbing CC (2006) The bactericidal agent triclosan modulates thyroid hormone-associated gene expression and disrupts postembryonic anuran development. Aquat Toxicol 80:217–227

    Article  CAS  Google Scholar 

  • Vieira LR, Gravato C, Soares AM, Morgado F, Guilhermino L (2009) Acute effects of copper and mercury on the estuarine fish Pomatoschistus microps: linking biomarkers to behaviour. Chemosphere 76(10):1416–1427. https://doi.org/10.1016/j.chemosphere.2009

    Article  CAS  Google Scholar 

  • Wang J, Pan L, Wu S, Lu L, Xu Y, Zhu Y, Guo M, Zhuang S (2016) Recent advances on endocrine disrupting effects of UV filters. Int J Environ Res Public Health 13(8):782. https://doi.org/10.3390/ijerph13080782

    Article  CAS  Google Scholar 

  • Wen Y, Schoups G, Giesen N (2017a) Organic pollution of rivers: Combined threats of urbanization, livestock farming and global climate change. Sci Rep 7:43289. https://doi.org/10.1038/srep43289

    Article  CAS  Google Scholar 

  • Wen B, Jin S-R, Chen ZZ, Gao J-Z, Wang L, Ying L, Liu Y, Liew H-P (2017b) Plasticity of energy reserves and metabolic performance of discus fish (Symphysodon aequifasciatus) exposed to low-temperature stress. Aquaculture 481:169–176. https://doi.org/10.1016/j.aquaculture.2017.09.002

    Article  Google Scholar 

  • Yamano K, Miwa S, Obinata T, Inui Y (1991) Thyroid hormone regulates developmental changes in muscle during flounder metamorphosis. Gen Comp Endocrinol 81(3):464–472

    Article  CAS  Google Scholar 

  • Young AR (2006) Acute effects of UVR on human eyes and skin. Prog Biophys Mol Biol 92:80–85

    Article  CAS  Google Scholar 

  • Young AR, Claveau J, Rossi AB (2017) Ultraviolet radiation and the skin: Photobiology and sunscreen photoprotection. J Am Acad Dermatol 76(3S1):100–109

    Article  Google Scholar 

  • Yu L, Wan F, Dutta S, Welsh S, Liu Z, Freundt E, Baehrecke EH, Lenardo M (2006) Autophagic programmed cell death by selective catalase degradation. Proc Natl Acad Sci U S A 28 103(13):4952–4957. https://doi.org/10.1073/pnas.0511288103

  • Yue Z, Yu M, Zhang X, Dong Y, Tian H, Wang W, Ru S (2017) Semicarbazide-induced thyroid disruption in Japanese flounder (Paralichthys olivaceus) and its potential mechanisms. Ecotoxicol Environ Saf 140:131–140. https://doi.org/10.1016/j.ecoenv.2017.02.043

    Article  CAS  Google Scholar 

  • Yúfera M, Parra G, Santiago R, Carrascosa M (1999) Growth, carbon, nitrogen and caloric content of Solea senegalensis (Pisces: Soleidae) from egg fertilization to metamorphosis. Mar Biol 134:43–49

    Article  Google Scholar 

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Acknowledgements

Thanks are due to FCT/MCTES for the financial support to CESAM (UIDP/50017/2020+UIDB/50017/2020), through national funds. The work of MJA was supported by the Portuguese Foundation for Science and Technology (FCT) through the scholarship ref. SFRH/BD/52572/2014 and MSM is funded by national funds (OE), through FCT, I.P., in the scope of the framework contract foreseen in the numbers 4, 5 and 6 of the article 23, of the Decree-Law 57/2016, of August 29, changed by Law 57/2017, of July 19. The authors also acknowledge Sea8 for providing S. senegalensis eggs, MSc. Abel Ferreira for laboratory assistance and Dr. Rui Rocha and Dr. Ricardo Calado for all the technical support. The authors would also like to acknowledge Mick Mackey (IRMRS) for the English revision and the contribution of two anonymous reviewers.

Funding

Thanks are due for the financial support to CESAM (UIDP/50017/2020+UIDB/50017/2020), through national funds. The work of MJA was supported by Portuguese Foundation for Science and Technology (FCT) through the scholarship ref. SFRH/BD/52572/2014 and MSM is funded by national funds (OE), through FCT, I.P., in the scope of the framework contract foreseen in the numbers 4, 5 and 6 of the article 23, of the Decree-Law 57/2016, of August 29, changed by Law 57/2017, of July 19.

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Authors and Affiliations

  1. CESAM-Centre for Environmental and Marine Studies, Department of Biology, University of Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal

    Mário J. Araújo, Amadeu M. V. M. Soares & Marta S. Monteiro

  2. CIIMAR-Interdisciplinary Centre of Marine and Environmental Research of the University of Porto, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos s/n, 4450-208, Matosinhos, Portugal

    Mário J. Araújo

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  1. Mário J. Araújo
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  2. Amadeu M. V. M. Soares
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  3. Marta S. Monteiro
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Contributions

• Mário J. Araújo: conceptualization, methodology, investigation, writing-original draft preparation.

• Amadeu M.V.M. Soares: supervision, funding acquisition, project administration.

• Marta S. Monteiro: conceptualization, investigation, writing-reviewing and editing.

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Correspondence to Mário J. Araújo.

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Fig. S1

Metamorphosis progression of Solea senegalensis. Fish from solvent control group were exposed to ethanol in saltwater (0.01% v/v) at 13 days after hatching (dah) during 48h and then fish were maintained in clean medium until complete metamorphosis, at 24 dah. Data represent the percentage of fish in each development stage (A, B, C, D, E, F, and G stages as described in Supplementary Table S1) in each control group. * represent significant differences between solvent and negative control group for each same day (p<0.05, Chi-square Test). (JPG 83 kb)

Fig. S2

Behaviour of Solea senegalensis in each 15 min. light or dark cycle at the 60 min behavior test performed at the end of metamorphosis (24 days after hatching, dah): i) negative and solvent controls and ii) solvent control and 4-MBC treatment groups. Exposure to 4-MBC was performed at 13 dah during 48h and fish maintained in clean medium until complete metamorphosis (24 dah). Different upper case letters above each bar represent existence of significant differences between each period (p<0.05, Two-way Repeated Measures ANOVA). (JPG 317 kb)

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Araújo, M.J., Soares, A.M.V.M. & Monteiro, M.S. Effects of exposure to the UV-filter 4-MBC during Solea senegalensis metamorphosis. Environ Sci Pollut Res 28, 51440–51452 (2021). https://doi.org/10.1007/s11356-021-14235-4

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  • DOI: https://doi.org/10.1007/s11356-021-14235-4

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