Martínez, M.L.; Piol, M.N.; Sbarbati Nudelman, N.; Verrengia Guerrero, N.R."Tributyltin bioaccumulation and toxic effects in freshwater gastropods Pomacea canaliculata after a chronic exposure: field and laboratory studies" (2017) Ecotoxicology. 26(5):691-701
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Freshwater samples and gastropod mollusks (Pomacea canaliculata) were collected at 5 sampling stations located along the lower Río de la Plata basin, Argentina, to assess the extent of tributyltin (TBT) contamination. Determined data revealed the presence of TBT and some of its breakdown products (dibutyltin: DBT, and monobutyltin: MBT) in all freshwater samples and also in soft tissues of P. canaliculata gastropods. Chronic bioassays (6 months) were performed using female gastropods that had been reared under laboratory conditions and exposed to a similar TBT concentration than the value determined in freshwater samples (1 µg L−1). The aims of this study were to evaluate the extent of TBT accumulation, the tissue distribution, and the effects on selected biomarkers (activity of superoxide dismutasa: SOD, activity of catalase: CAT, levels of total glutathione: t-GSH, lipid peroxidation, and activity of acetylcholinesterase: AChE). Gonads presented the highest accumulation, followed by the cephalopedal region, albumin gland, and finally hepatopancreas. Both metabolites, DBT and MBT, were also found. All exposed female animals presented development of a penis reflecting the potential of TBT as an endocrine disrupting chemical for this gastropod species. Results on the selected biomarkers confirmed additional adverse effects induced by TBT. An increase in CAT activity and changes in t-GSH levels are indicative of alterations on the cellular redox status. The inhibition of AChE could reflect signs of neurotoxicity. Altogether, these results reveal a negative impact on the health of this gastropod population. © 2017, Springer Science+Business Media New York.


Documento: Artículo
Título:Tributyltin bioaccumulation and toxic effects in freshwater gastropods Pomacea canaliculata after a chronic exposure: field and laboratory studies
Autor:Martínez, M.L.; Piol, M.N.; Sbarbati Nudelman, N.; Verrengia Guerrero, N.R.
Filiación:Facultad de Ciencias Exactas y Naturales, Dpto. de Química Orgánica, Universidad de Buenos Aires, 3° piso, Pabellón II, Buenos Aires, Argentina
Facultad de Ciencias Exactas y Naturales, Dpto. de Química Biológica, Toxicología y Química Legal, Universidad de Buenos Aires, 4° piso, Pabellón II, Buenos Aires, Argentina
Palabras clave:Biomarkers; Female gastropods; Freshwater systems; Pomacea canaliculata; TBT; acetylcholinesterase; biological marker; catalase; dibutyltin; fresh water; glutathione; monobutyltin; organotin compound; superoxide dismutase; tributyltin; unclassified drug; tributyltin; water pollutant; bioaccumulation; biomarker; endocrine disruptor; freshwater ecosystem; snail; toxicity; tributyltin; animal experiment; animal tissue; Argentina; Article; bioaccumulation; controlled study; enzyme activity; enzyme inhibition; female; field study; gastropod; gonad; hepatopancreas; laboratory test; lipid peroxidation; long term exposure; neurotoxicity; nonhuman; organogenesis; oxidation reduction state; penis; Pomacea canaliculata; priority journal; redox stress; river basin; tissue distribution; tissue level; water contamination; animal; environmental monitoring; gastropod; metabolism; physiology; toxicity; toxicity testing; water pollutant; Argentina; Rio de la Plata; Animalia; Gastropoda; Mollusca; Pomacea canaliculata; Animals; Environmental Monitoring; Gastropoda; Toxicity Tests, Chronic; Trialkyltin Compounds; Water Pollutants, Chemical
Página de inicio:691
Página de fin:701
Título revista:Ecotoxicology
Título revista abreviado:Ecotoxicology
CAS:acetylcholinesterase, 9000-81-1; catalase, 9001-05-2; dibutyltin, 1002-53-5; glutathione, 70-18-8; superoxide dismutase, 37294-21-6, 9016-01-7, 9054-89-1; tributyltin, 688-73-3; Trialkyltin Compounds; tributyltin; Water Pollutants, Chemical


  • Abele, D., Vazquez-Medina, J.P., Zenteno-Savin, T., (2012) Oxidative stress in aquatic ecosystems, , Wiley-Blackwell, Chichester, West Sussex
  • Alves Costa, J.R.M., Mela, M., da Silva de Assis, H.C., Pelletier, E., Ferreira Randi, M.A., Oliveira Ribeiro, C.A., Enzymatic inhibition and morphological changes in Hoplias malabaricus from dietary exposure to lead(II) or methylmercury (2007) Ecotox Environ Safe, 67, pp. 82-88. , COI: 1:CAS:528:DC%2BD2sXjvFGms7s%3D
  • Arp, H.P.H., Eek, E., Nybakk, A.W., Glette, T., Møskeland, T., Pettersen, A., When will the TBT go away? Integrating monitoring and modelling to address TBT’s delayed disappearance in the Drammensfjord, Norway (2014) Water Res, 65, pp. 213-223. , COI: 1:CAS:528:DC%2BC2cXht1Ghu7bN
  • Axiak, V., Vella, A.J., Agius, D., Bonnici, P., Cassar, G., Cassoe, R., Chircop, P., Sammut, M., Evaluation of environmental levels and biological impact of TBT in Malta (central Mediterranean) (2000) Sci Total Environ, 258, pp. 89-97. , COI: 1:CAS:528:DC%2BD3cXlvVCksb8%3D
  • Batista, R.M., Castro, I.B., Fillmann, G., Imposex and butyltin contamination still evident in Chile after TBT global ban (2016) Sci Total Environ, 566-567, pp. 446-453. , COI: 1:CAS:528:DC%2BC28XoslWrur0%3D
  • Bernanke, J., Köhler, H.R., The impact of environmental chemicals on wildlife vertebrates (2009) Rev Environ Contam Toxicol, 198, pp. 1-47. , COI: 1:CAS:528:DC%2BD1MXhtVahs78%3D
  • Bigatti, G., Averbuj, A., Braga Castro, I., Primost, M., Carranza, A., Commendatore, M., Fillmann, G., Penchaszadeh, P.E., Situación de contaminación en las costas del sur de Brazil, Uruguay y Argentina luego de la prohibición mundial de TBT (2014) Nuevas miradas a la problemática de los ambientes costeros. Difusión, Relaciones y Actividades Culturales (DIRAC) – Facultad de Ciencias, Montevideo, Uruguay, pp. 277-301. , Goso C, (ed), pp
  • Buggy, C.J., Tobin, J.M., Seasonal and spatial distributions of tributyltin in surface sediment of the Tolka Estuary, Dublin, Ireland (2006) Environ Pollut, 143, pp. 294-303. , COI: 1:CAS:528:DC%2BD28Xks1OlsL4%3D
  • Castro, I.B., Arroyo, M., Costa, P., Fillmann, G., Butyltin compounds and imposex levels in Ecuador (2012) Arch Environ Contam Toxicol, 62, pp. 68-77. , COI: 1:CAS:528:DC%2BC3MXhs1KrsbjJ
  • Cazzaniga, N.J., Sexual dimorphism in Pomacea canaliculata (1990) Veliger, 33, pp. 390-394
  • Claiborne, A., Catalase activity (1985) CRC handbook of methods for oxygen radical research, pp. 283-284. , Greenwald R, (ed), CRC Press, Boca Raton, FL: pp
  • Couceiro, L., Díaz, J., Albaina, N., Barreiro, R., Irabien, J.A., Ruiz, J.M., Imposex and gender-independent butyltin accumulation in the gastropod Nassarius reticulatus from the Cantabrian coast (N Atlantic Spain) (2009) Chemosphere, 76, pp. 424-427. , COI: 1:CAS:528:DC%2BD1MXmtl2rtbY%3D
  • Devier, M.H., Augagneur, S., Budzinski, H., Mora, P., Narbonne, J.F., Garrigues, P., Microcosm tributyltin bioaccumulation and multibiomarker assessment in the blue mussel Mytilus edulis (2003) Environ Toxicol Chem, 22, pp. 2679-2687. , COI: 1:CAS:528:DC%2BD3sXotFOgs7k%3D
  • Dickinson, D.A., Forman, H.J., Cellular glutathione and thiols metabolism (2002) Biochem Pharmacol, 64, pp. 1019-1026. , COI: 1:CAS:528:DC%2BD38Xms1ymsb4%3D
  • Dowson, P.H., Bubb, J.M., Lester, J.N., Persistence and degradation pathways of tributyltin in freshwater and estuarine sediments (1996) Estuar Coast Shelf S, 42, pp. 551-562. , COI: 1:CAS:528:DyaK28Xjs1CjtLc%3D
  • Ellman, G.L., Courtney, K.D., Andres, V., Jr., Featherstone, R.M., A new and rapid colorimetric determination of acetylcholinesterase activity (1961) Biochem Pharmacol, 7, pp. 88-95. , COI: 1:CAS:528:DyaF3MXht1Gns7o%3D
  • Fent, K., Ecotoxicology of organotin compounds (1996) Crit Rev Toxicol, 26, pp. 1-117. , COI: 1:CAS:528:DyaK28XhtFyhur8%3D
  • Fent, K., Weston, A.A., Caminada, D., Ecotoxicology of human pharmaceuticals (2006) Aquat Toxicol, 73, pp. 122-159
  • Giraud-Billoud, M., Vega, I.A., Wuilloud, R.G., Clément, M.E., Castro-Vazquez, A., Imposex and novel mechanisms of reproductive failure induced by tributyltin (TBT) in the freshwater snail Pomacea canaliculata (2013) Environ Toxicol Chem, 32, pp. 2365-2371. , COI: 1:CAS:528:DC%2BC3sXhtlOku7jM
  • (2016) GISD: Global Invasive Species Database, ,, Accessed 22 October 2016
  • Hermes-Lima, M., Storey, J.M., Storey, K.B., Antioxidant defenses and metabolic depression. The hypothesis of preparation for oxidative stress in land snails (1998) Comp Biochem Phys Part B, 120, pp. 437-448. , COI: 1:STN:280:DyaK1M%2FgsVSksA%3D%3D
  • Higuera-Ruiz, R., Elorza, J., Shell thickening and chambering in the oyster Crassostrea gigas: natural and anthropogenic influence of tributyltin contamination (2011) Environ Technol, 32, pp. 583-591. , COI: 1:CAS:528:DC%2BC3MXntlSls74%3D
  • Hoch, M., Organotin compounds in the environment-an overview (2001) Appl Geochem, 16, pp. 719-743. , COI: 1:CAS:528:DC%2BD3MXisVWjt7k%3D
  • Jagtap, J.T., Shejule, K.B., Jaiswal, D.P., Acute toxicity study of tributyltin chloride on the freshwater bivalve, Lamellidens marginalis (2011) World J Fish Marine Sci, 3, pp. 100-103. , COI: 1:CAS:528:DC%2BC3MXmtFWhsrs%3D
  • Kim, B.M., Rhee, J.S., Park, G.S., Lee, J., Lee, Y.M., Lee, J.S., Cu/Zn- and Mn-superoxide dismutase (SOD) from the copepod Tigriopus japonicus: Molecular cloning and expression in response to environmental pollutants (2011) Chemosphere, 84, pp. 1467-1475. , COI: 1:CAS:528:DC%2BC3MXhtVagtLbF
  • Labrot, F., Ribera, D., Saint Denis, M., Narbonne, J.F., In vitro and in vivo studies of potential biomarkers of lead and uranium contamination: lipid peroxidation, acetylcholinesterase, catalase and glutathione peroxidase activities in three non-mammalian species (1996) Biomarkers, 1, pp. 21-28. , COI: 1:CAS:528:DyaK28XivVGjtro%3D
  • Láng, G., Kufcsák, O., Szegletes, T., Nemcsók, J., Quantitive distributions of different cholinesterases and inhibition of acetylcholinesterase by metidathion and paraquat in alimentary canal of common carp (1997) Gen Pharmac, 29, pp. 55-59
  • Lesser, M.P., Oxidative stress in marine environments: biochemistry and physiological ecology (2006) Annu Rev Physiol, 68, pp. 253-278. , COI: 1:CAS:528:DC%2BD28XksFWksrY%3D
  • Leung, K., Grist, E., Morley, N., Morritt, D., Crane, M., Chronic toxicity of tributyltin to development and reproduction of the European freshwater snail Lymnaea stagnalis (L.) (2007) Chemosphere, 66, pp. 1358-1366. , COI: 1:CAS:528:DC%2BD28XhtlSiu77K
  • Liu, W.H., Chiu, Y.W., Huang, D.J., Liu, M.Y., Lee, C.C., Liu, L.L., Imposex in the golden apple snail Pomacea canaliculata in Taiwan (2006) Sci Total Environ, 371, pp. 138-143. , COI: 1:CAS:528:DC%2BD28XhtFOrtbrJ
  • Lowry, O.H., Rosebrough, A., Farr, L., Randall, R.S., Protein measurement with the folin phenol reagent (1951) J Biol Chem, 249, pp. 265-275
  • Lushchak, V.I., Environmentally induced oxidative stress in aquatic animals (2011) Aquat Toxicol, 101, pp. 13-30. , COI: 1:CAS:528:DC%2BC3cXhsFGgsLjJ
  • Martins, S.E., Bianchini, A., Toxicity tests aiming to protect Brazilian aquatic systems: current status and implications for management (2011) J Environ Monitor, 13, pp. 1866-1875. , COI: 1:CAS:528:DC%2BC3MXosVCru7Y%3D
  • Matthiessen, P., Detection, monitoring, and control of tributyltin - an almost complete success story (2013) Environ Toxicol Chem, 32, pp. 487-489. , COI: 1:CAS:528:DC%2BC3sXivVyrtbk%3D
  • Misra, H.P., Fridovich, I., The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase (1972) J Biol Chem, 247, pp. 3170-3175. , COI: 1:CAS:528:DyaE38XhsFSntLk%3D
  • Mitra, S., Gera, R., Siddiquib, W.A., Khandelwal, S., Tributyltin induces oxidative damage, inflammation and apoptosis via disturbance in blood–brain barrier and metal homeostasis in cerebral cortex of rat brain: an in vivo and in vitro study (2013) Toxicology, 310, pp. 39-52. , COI: 1:CAS:528:DC%2BC3sXht1Shs7vJ
  • Nakayama, K., Oshima, Y., Tachibana, T., Furuse, M., Honjo, T., Alteration of monoamine concentrations in the brain of medaka, Oryzias latipes, exposed to tributyltin (2007) Environ Toxicol, 22, pp. 53-57. , COI: 1:CAS:528:DC%2BD2sXisFCrsrs%3D
  • Pagliarani, A., Nesci, S., Ventrella, V., Toxicity of organotin compounds: shared and unshared biochemical targets and mechanisms in animal cells (2013) Toxicol in Vitro, 27, pp. 978-990. , COI: 1:CAS:528:DC%2BC3sXjvV2ltA%3D%3D
  • Paz-Villarraga, C.A., Castro, I.B., Miloslavich, P., Fillmann, G., Venezuelan Caribbean Sea under the threat of TBT (2015) Chemosphere, 119, pp. 704-710. , COI: 1:CAS:528:DC%2BC2cXht12ntb7F
  • Pinochet, H., Tessini, C., Bravo, M., Quiroz, W., De Gregori, I., Butyltin compounds and their relation with organic matter in marine sediments from San Vicente Bay, Chile (2009) Environ Monit Assess, 155, pp. 341-353. , COI: 1:CAS:528:DC%2BD1MXotlOrurg%3D
  • (1998) Régimen para la protección del medioambiente. Ordenanza No 4/98, , Buenos Aires, Argentina
  • Quintas, P.Y., Oliva, A.L., Arias, A., Domini, C.E., Alvarez, M.B., Garrido, M., Marcovecchio, J.E., Seasonal changes in organotin compounds in sediments from the Bahía Blanca Estuary (2016) Environ Earth Sci, 75, pp. 659-671
  • Rabitto, I.S., Alves Costa, J.R.M., Silva de Assis, H.C., Pelletier, É., Akaishi, F.M., Anjos, A., Randi, M.A.F., Oliveira Ribeiroa, C.A., Effects of dietary Pb(II) and tributyltin on neotropical fish, Hoplias malabaricus: histopathological and biochemical findings (2005) Ecotox Environ Safe, 60, pp. 147-156. , COI: 1:CAS:528:DC%2BD2cXpslWntbo%3D
  • Rand, G.M., (1995) Fundamentals of aquatic toxicology: effects, environmental fate, and risk assessment, , Taylor & Francis, London
  • Rodríguez Grimón, R.O., Arroyo Osorio, M.F., de Freitas, D.M., Castro, I.B., Tributyltin impacts in Galapagos Islands and Ecuadorian shore: marine protected areas under threat (2016) Marine Policy, 69, pp. 24-31
  • Rüdel, H., Case study: bioavailability of tin and tin compounds (2003) Ecotox Environ Safe, 56, pp. 180-189
  • Sternberg, R.M., Gooding, M.P., Hotchkiss, A.K., LeBlanc, G.A., Environmental-endocrine control of reproductive maturation in gastropods: implications for the mechanism of tributyltin induced imposex in prosobranchs (2009) Ecotoxicology, 19, pp. 4-23
  • Tallarico, L.F., Freshwater gastropods as a tool for ecotoxicology assessments in Latin America (2016) Amer Malac Bull, 33, pp. 330-336
  • Tessier, E., Amouroux, D., Morin, A., Christian, L., Thybaud, E., Vindimian, E., Donard, O.F.X., Tri)Butyltin biotic degradation rates and pathways in different compartments of a freshwater model ecosystem (2007) Sci Total Environ, 388, pp. 214-233. , COI: 1:CAS:528:DC%2BD2sXht1ShtLnJ
  • Tietze, F., Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues (1969) Anal Biochem, 27, pp. 502-522. , COI: 1:CAS:528:DyaF1MXktVSlt7k%3D
  • Tsunoda, M., Konno, N., Nakano, K., Liu, Y., Altered metabolism of dopamine in the midbrain of mice treated with tributyltin chloride via subacute oral exposure (2004) Environ Sci, 11, pp. 209-219. , COI: 1:CAS:528:DC%2BD2cXos1yls7k%3D
  • Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms, 5th edition. EPA-821-R-02-012 (2002) United States Environmnental Protecion Agency, , Washington, DC: USA
  • Ambient aquatic life water quality criteria for tributyltin (TBT) – Final. EPA 822-R-03-031 (2003) United States Environmnental Protecion Agency, , Washington, DC: USA
  • Valavanidis, A., Vlahogianni, T., Dassenakis, M., Scoullos, M., Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants (2006) Ecotox Environ Safe, 64, pp. 178-189. , COI: 1:CAS:528:DC%2BD28XltFCmsLo%3D
  • Waisbaum, R.G., Rodriguez, C., Nudelman, N.S., Determination of TBT in water and sediment samples along the Argentine Atlantic coast (2010) Environ Technol, 31, pp. 1335-1342
  • Wang, C.G., Chen, Y.X., Li, Y., Wei, W., Yu, Q., Effects of low dose tributyltin on activities of hepatic antioxidant and phase II enzymes in Sebastiscus marmoratus (2005) Bull Environ Contam Toxicol, 74, pp. 114-119. , COI: 1:CAS:528:DC%2BD2MXmtlCqtQ%3D%3D
  • Wang, X., Fang, C., Hong, H., Wang, W.X., Gender differences in TBT accumulation and transformation in Thais clavigera after aqueous and dietary exposure (2010) Aquat Toxicol, 99, pp. 413-422. , COI: 1:CAS:528:DC%2BC3cXpsFKitr4%3D
  • Wang, X.H., Hong, H.S., Zhao, D.M., Hong, L.Y., Environmental behavior of organotin compounds in the costal environment of Xiamen, China (2008) Mar Poll Bull, 57, pp. 419-424. , COI: 1:CAS:528:DC%2BD1cXntlGmsLk%3D
  • Zhou, J., Zhu, X., Cai, Z., Tributyltin toxicity in abalone (Haliotis diversicolor supertexta) assessed by antioxidant enzyme activity, metabolic response, and histopathology (2010) J Hazard Mater, 183, pp. 428-433. , COI: 1:CAS:528:DC%2BC3cXhtFChtrrN


---------- APA ----------
Martínez, M.L., Piol, M.N., Sbarbati Nudelman, N. & Verrengia Guerrero, N.R. (2017) . Tributyltin bioaccumulation and toxic effects in freshwater gastropods Pomacea canaliculata after a chronic exposure: field and laboratory studies. Ecotoxicology, 26(5), 691-701.
---------- CHICAGO ----------
Martínez, M.L., Piol, M.N., Sbarbati Nudelman, N., Verrengia Guerrero, N.R. "Tributyltin bioaccumulation and toxic effects in freshwater gastropods Pomacea canaliculata after a chronic exposure: field and laboratory studies" . Ecotoxicology 26, no. 5 (2017) : 691-701.
---------- MLA ----------
Martínez, M.L., Piol, M.N., Sbarbati Nudelman, N., Verrengia Guerrero, N.R. "Tributyltin bioaccumulation and toxic effects in freshwater gastropods Pomacea canaliculata after a chronic exposure: field and laboratory studies" . Ecotoxicology, vol. 26, no. 5, 2017, pp. 691-701.
---------- VANCOUVER ----------
Martínez, M.L., Piol, M.N., Sbarbati Nudelman, N., Verrengia Guerrero, N.R. Tributyltin bioaccumulation and toxic effects in freshwater gastropods Pomacea canaliculata after a chronic exposure: field and laboratory studies. Ecotoxicology. 2017;26(5):691-701.