[en] Thyroid hormones are critically involved in somatic growth, development and metamorphosis of vertebrates. The structural similarity between thyroid hormones and triclosan, an antimicrobial compound widely employed in consumer personal care products, suggests triclosan can have adverse effects on the thyroid system. The sheepshead minnow, Cyprinodon variegatus, is now used in ecotoxicological studies that have recently begun to focus on potential disruption of the thyroid axis by endocrine disrupting compounds. Here, we investigate the in vivo effects of exposure to triclosan (20, 50, and 100 μg L−1) on the thyroid system and the embryonic and larval development of C. variegatus. Triclosan exposure did not affect hatching success, but delayed hatching time by 6–13 h compared to control embryos. Triclosan exposure affected the ontogenetic variations of whole body thyroid hormone concentrations during the larval phase. The T3 peak around 12–15 dph, described to be indicative for the metamorphosis climax in C. variegatus, was absent in triclosan-exposed larvae. Triclosan exposure did not produce any deformity or allometric repatterning, but a delayed development of 18–32 h was observed. We conclude that the triclosan-induced disruption of the thyroid system delays in vivo the start of metamorphosis in our experimental model. We observed a global developmental delay of 24–45 h, equivalent to 4–7% prolongation of the developmental time in C. variegatus. The costs of delayed metamorphosis can lead to reduction of juvenile fitness and could be a determining factor in the outcome of competitive interactions.
Centre/Unité de recherche :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège
Disciplines :
Sciences de l’environnement & écologie Sciences aquatiques & océanologie
Auteur, co-auteur :
Schnitzler, Joseph ; Université de Liège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Frederich, Bruno ; Université de Liège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Dussenne, Mélanie ; Université de Liège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Klaren, Peter
Silvestre, Frédéric
Das, Krishna ; Université de Liège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Langue du document :
Anglais
Titre :
Triclosan exposure results in alterations of thyroid hormone status and retarded early development and metamorphosis in Cyprinodon variegatus
Allen, B.M., The results of thyroid removal in the larvae of Rana pipiens. J. Exp. Zool. 24 (1918), 499–519.
Axelstad, M., Boberg, J., Vinggaard, A.M., Christiansen, S., Hass, U., Triclosan exposure reduces thyroxine levels in pregnant and lactating rat dams and in directly exposed offspring. Food Chem. Toxicol. 59 (2013), 534–540.
Bedoux, G., Roig, B., Thomas, O., Dupont, V., Le Bot, B., Occurrence and toxicity of antimicrobial triclosan and by-products in the environment. Environ. Sci. Pollut. Res., 2011, 1–22.
Bernier, N.J., Flik, G., Klaren, P.H., Regulation and contribution of the corticotropic, melanotropic and thyrotropic axes to the stress response in fishes. Fish Physiol. 28 (2009), 235–311.
Blanton, M.L., Specker, J.L., The Hypothalamic-Pituitary-Thyroid (HPT) axis in fish and its role in fish development and reproduction. Crit. Rev. Toxicol. 37 (2007), 97–115.
Boas, M., Feldt-Rasmussen, U., Skakkebaek, N.E., Main, K.M., Environmental chemicals and thyroid function. Eur. J. Endocrinol. 154 (2006), 599–611.
Bookstein, F.L., Combining the tools of geometric morphometrics Advances in morphometrics. 1996, Springer, 131–151.
Bookstein, F.L., Morphometric Tools for Landmark Data: Geometry and Biology. 1997, University Press, Cambridge.
Brännäs, E., Influence of photoperiod and temperature on hatching and emergence of Baltic salmon (Salmo salar L.). Can. J. Zool. 65 (1987), 1503–1508.
Brown, S.B., Adams, B.A., Cyr, D.G., Eales, J.G., Contaminant effects on the teleost fish thyroid. Environ. Toxicol. Chem. 23 (2004), 1680–1701.
Butt, C.M., Wang, D., Stapleton, H.M., Halogenated phenolic contaminants inhibit the in vitro activity of the thyroid regulating deiodinases in human liver. Toxicol. Sci. 124 (2011), 339–347.
Chang, J., Wang, M., Gui, W., Zhao, Y., Yu, L., Zhu, G., Changes in thyroid hormone levels during zebrafish development. Zoolog. Sci. 29 (2012), 181–184.
Cowen, R.K., Variation in the planktonic larval duration of the temperate wrasse Semicossyphus pulcher. Mar. Ecol. Prog. Ser. 69 (1991), 9–15.
Crane, H.M., Pickford, D.B., Hutchinson, T.H., Brown, J.A., Developmental changes of thyroid hormones in the fathead minnow, Pimephales promelas. Gen. Comp. Endocrinol. 139 (2004), 55–60.
Cripe, G.M., Hemmer, B.L., Goodman, L.R., Vennari, J.C., Development of a methodology for successful multigeneration life-cycle testing of the estuarine sheepshead minnow, Cyprinodon variegatus. Arch. Environ. Contam. Toxicol. 56 (2009), 500–508.
Crofton, K.M., Paul, K.B., DeVito, M.J., Hedge, J.M., Short-term in vivo exposure to the water contaminant triclosan: evidence for disruption of thyroxine. Environ. Toxicol. Pharmacol. 24 (2007), 194–197.
Dann, A.B., Hontela, A., Triclosan: environmental exposure, toxicity and mechanisms of action. J. Appl. Toxicol., 31, 2011, 285.
Dodd, M., Dodd, J., The biology of metamorphosis. Physiol. Amphibia 3 (1976), 467–599.
Dufour, S., Rousseau, K., Kapoor, B.G., Metamorphosis in Fish. 2012, CRC Press.
Eales, J.G., Brown, S.B., Measurement and regulation of thyroidal status in teleost fish. Rev. Fish Biol. Fish. 3 (1993), 299–347.
Fang, J.-L., Stingley, R.L., Beland, F.A., Harrouk, W., Lumpkins, D.L., Howard, P., Occurrence, efficacy, metabolism, and toxicity of triclosan. J. Environ. Sci. Health Part C Environ. Carcinog. Ecotoxicol. Rev. 28 (2010), 147–171.
Fort, D.J., Rogers, R.L., Gorsuch, J.W., Navarro, L.T., Peter, R., Plautz, J.R., Triclosan and anuran metamorphosis: no effect on thyroid-mediated metamorphosis in Xenopus laevis. Toxicol. Sci. 113 (2009), 392–400.
Hallare, A., Nagel, K., Köhler, H.-R., Triebskorn, R., Comparative embryotoxicity and proteotoxicity of three carrier solvents to zebrafish (Danio rerio) embryos. Ecotoxicol. Environ. Saf. 63 (2006), 378–388.
Inui, Y., Yamano, K., Miwa, S., The role of thyroid hormone in tissue development in metamorphosing flounder. Aquaculture 135 (1995), 87–98.
Ishibashi, H., Matsumura, N., Hirano, M., Matsuoka, M., Shiratsuchi, H., Ishibashi, Y., Takao, Y., Arizono, K., Effects of triclosan on the early life stages and reproduction of medaka Oryzias latipes and induction of hepatic vitellogenin. Aquat. Toxicol. 67 (2004), 167–179.
Jenkins, G.P., May, H., Variation in settlement and larval duration of king george whiting sillaginodes punctata (Sillaginidae), in swan bay victoria, Australia. Bull. Mar. Sci. 54 (1994), 281–296.
Johns, S.M., Kane, M.D., Denslow, N.D., Watanabe, K.H., Orlando, E.F., Villeneuve, D.L., Ankley, G.T., Sepulveda, M.S., Characterization of ontogenetic changes in gene expression in the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem. 28 (2009), 873–880.
Kawakami, Y., Tanda, M., Adachi, S., Yamauchi, K., Characterization of thyroid hormone receptor α and β in the metamorphosing Japanese conger eel, Conger myriaster. Gen. Comp. Endocrinol. 132 (2003), 321–332.
Klaren, P.H.M., Wunderink, Y.S., Yufera, M., Mancera, J.M., Flik, G., The thyroid gland and thyroid hormones in Senegalese sole (Solea senegalensis) during early development and metamorphosis. Gen. Comp. Endocrinol. 155 (2008), 686–694.
Klingenberg, C.P., McIntyre, G.S., Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution, 1998, 1363–1375.
Kolpin, D.W., Furlong, E.T., Meyer, M.T., Thurman, E.M., Zaugg, S.D., Barber, L.B., Buxton, H.T., Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams: 1999–2000: A national reconnaissance. Environ. Sci. Technol. 36 (2002), 1202–1211.
Lallemand, L., Voisin, A.-S., Darchambeau, F., Das, K., Schnitzler, J., The effects of Triclosan on the metabolism of developing Sheepshead minnow (Cyprinodon variegatus) larvae. ZOOLOGY 2014-Congrès Benelux de Zoologie, 2014.
Laudet, V., The origins and evolution of vertebrate metamorphosis. Curr. Biol. 21 (2011), R726–R737.
Lawing, A.M., Polly, P.D., Geometric morphometrics: recent applications to the study of evolution and development. J. Zool. 280 (2010), 1–7.
Leatherland, J.F., Environmental physiology of the teleostean thyroid gland: a review. Environ. Biol. Fishes 7 (1982), 83–110.
Lecchini, D., Galzin, R., Spatial repartition and ontogenetic shifts in habitat use by coral reef fishes (Moorea, French Polynesia). Mar. Biol. 147 (2005), 47–58.
McCormick, M.I., Delayed metamorphosis of a tropical reef fish (Acanthurus triostegus): a field experiment. Mar. Ecol. Prog. Ser. 176 (1999), 25–38.
Nassef, M., Kim, S.G., Seki, M., Kang, I.J., Hano, T., Shimasaki, Y., Oshima, Y., In ovo nanoinjection of triclosan, diclofenac and carbamazepine affects embryonic development of medaka fish (Oryzias latipes). Chemosphere 79 (2010), 966–973.
OECD, OECD guidelines for testing of chemicals: fish, early-life stage toxicity test. OECD Publ., 2013.
Oliveira, R., Domingues, I., Grisolia, C.K., Soares, A.M.V.M., Effects of triclosan on zebrafish early-life stages and adults. Environ. Sci. Pollut. Res. 16 (2009), 679–688.
Orvos, D.R., Versteeg, D.J., Inauen, J., Capdevielle, M., Rothenstein, A., Cunningham, V., Aquatic toxicity of triclosan. Environ. Toxicol. Chem. 21 (2002), 1338–1349.
Osse, J., Van den Boogaart, J., Size of flatfish larvae at transformation, functional demands and historical constraints. J. Sea Res. 37 (1997), 229–239.
Paris, M., Laudet, V., The history of a developmental stage: metamorphosis in chordates. Genesis 46 (2008), 657–672.
Paul, K.B., Hedge, J.M., Devito, M.J., Crofton, K.M., Short-term exposure to triclosan decreases thyroxine in vivo via upregulation of hepatic catabolism in young long-evans rats. Toxicol. Sci. 113 (2009), 367–379.
Pechenik, J.A., Larval experience and latent effects—metamorphosis is not a new beginning. Integr. Comp. Biol. 46 (2006), 323–333.
Pinto, P.I., Guerreiro, E.M., Power, D.M., Triclosan interferes with the thyroid axis in the zebrafish (Danio rerio). Toxicol. Res. 2 (2013), 60–69.
Power, D.M., Llewellyn, L., Faustino, M., Nowell, M.A., Björnsson, B.T., Einarsdottir, I.E., Canario, A.V.M., Sweeney, G.E., Thyroid hormones in growth and development of fish. Comp. Biochem. Physiol. Part C: Toxicol. Pharmacol. 130 (2001), 447–459.
R Development Core Team, R: A Language and Environment for Statistical Computing R Foundation for Statistical Computing. 2014, R Foundation for Statistical Computing, Vienna, Austria.
Rohlf, F.J., Slice, D., Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst. Biol. 39 (1990), 40–59.
Schnitzler, J.G., Klaren, P.H.M., Mariavelle, E., Das, K., The thyroid gland and thyroid hormones in sheepshead minnow (Cyprinodon variegatus) during early development and metamorphosis. Fish. Physiol. Biochem. 42 (2015), 607–616.
Schnitzler, J.G., Dussenne, M., Frédérich, B., Das, K., Post-embryonic development of sheepshead minnow Cyprinodon variegatus: a staging tool based on externally visible anatomical traits. Ichthyol. Res. 64 (2016), 1–8.
Schuur, A.G., van Leeuwen-Bol, I., Jong, W.M., Bergman, Å., Coughtrie, M.W., Brouwer, A., Visser, T.J., In vitro inhibition of thyroid hormone sulfation by polychlorobiphenylols: isozyme specificity and inhibition kinetics. Toxicol. Sci. 45 (1998), 188–194.
Searcy, S.P., Sponaugle, S., Selective mortality during the larval-juvenile transition in two coral reef fishes. Ecology 82 (2001), 2452–2470.
Sheets, H., Regress8: calculation of regressions between shape variables and a dependant variable. Buffalo, 2014.
Shiao, J.-C., Wu, S.-M., Hwang, Y.-P., Wu, D.-P., Hwang, P.-P., Evaluation of thyroid-mediated otolith growth of larval and juvenile tilapia. J. Exp. Biol. 211 (2008), 1919–1926.
Shima, J.S., Findlay, A.M., Pelagic larval growth rate impacts benthic settlement and survival of a temperate reef fish. Mar. Ecol. Prog. Ser. 235 (2002), 303–309.
Stoker, T.E., Gibson, E.K., Zorrilla, L.M., Triclosan exposure modulates estrogen-dependent responses in the female Wistar rat. Toxicol. Sci. 117 (2010), 45–53.
Szisch, V., Papandroulakis, N., Fanouraki, E., Pavlidis, M., Ontogeny of the thyroid hormones and cortisol in the gilthead sea bream, Sparus aurata. Gen. Comp. Endocrinol. 142 (2005), 186–192.
Tagawa, M., Hirano, T., Presence of thyroxine in eggs and changes in its content during early development of chum salmon, Oncorhynchus keta. Gen. Comp. Endocrinol. 68 (1987), 129–135.
Victor, B.C., Delayed metamorphosis with reduced larval growth in aCoral reef fish (Thalassoma bifasciatum). Can. J. Fish. Aquat.Sci. 43 (1986), 1208–1213.
Villamizar, N., Blanco-Vives, B., Oliveira, C., Dinis, M.T., Di Rosa, V., Negrini, P., Bertolucci, C., Sánchez-Vázquez, F.J., Circadian rhythms of embryonic development and hatching in fish: a comparative study of Zebrafish (diurnal), Senegalese sole (nocturnal), and Somalian cavefish (blind). Chronobiol. Int. 30 (2013), 889–900.
Webster, M., Zelditch, M.L., Evolutionary modifications of ontogeny: heterochrony and beyond. Paleobiology 31 (2005), 354–372.
Yamano, K., The role of thyroid hormone in fish development with reference to aquaculture. JARQ-Japan Agricult. Res. Q. 39 (2005), 161–168.
Zelditch, M.L., Lundrigan, B.L., Garland, T., Developmental regulation of skull morphology: I. Ontogenetic dynamics of variance. Evol. Dev.t 6 (2004), 194–206.
Zelditch, M.L., Swiderski, D.L., Sheets, H.D., Geometric Morphometrics for Biologists: a Primer. 2012, Academic Press.
Zoeller, R.T., Tan, S.T., Tyl, R.W., General background on the Hypothalamic-Pituitary-Thyroid (HPT) axis. Crit. Rev. Toxicol. 37 (2007), 11–53.
Zorrilla, L.M., Gibson, E.K., Jeffay, S.C., Crofton, K.M., Setzer, W.R., Cooper, R.L., Stoker, T.E., The effects of triclosan on puberty and thyroid hormones in male Wistar rats. Toxicol. Sci. 107 (2009), 56–64.
de Jesus, E.G.T., Hirano, T., Changes in whole body concentrations of cortisol, thyroid hormones, and sex steroids during early development of the chum salmon, Oncorhynchus keta. Gen. Comp. Endocrinol. 85 (1992), 55–61.
van der Veer, H.W., Nash, R.D., The 1999 Flatfish Symposium: where to go from now?. J. Sea Res. 45 (2001), 325–328.
