Abstract
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.
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Abele D, Vazquez-Medina JP, Zenteno-Savin T (2012) Oxidative stress in aquatic ecosystems. Wiley-Blackwell, Chichester, West Sussex
Alves Costa JRM, Mela M, da Silva de Assis HC, Pelletier E, Ferreira Randi MA, Oliveira Ribeiro CA (2007) Enzymatic inhibition and morphological changes in Hoplias malabaricus from dietary exposure to lead(II) or methylmercury. Ecotox Environ Safe 67:82–88
Arp HPH, Eek E, Nybakk AW, Glette T, Møskeland T, Pettersen A (2014) When will the TBT go away? Integrating monitoring and modelling to address TBT’s delayed disappearance in the Drammensfjord, Norway. Water Res 65:213–223
Axiak V, Vella AJ, Agius D, Bonnici P, Cassar G, Cassoe R, Chircop P, Micallef D, Mintoff B, Sammut M (2000) Evaluation of environmental levels and biological impact of TBT in Malta (central Mediterranean). Sci Total Environ 258:89–97
Batista RM, Castro IB, Fillmann G (2016) Imposex and butyltin contamination still evident in Chile after TBT global ban. Sci Total Environ 566-567:446–453
Bernanke J, Köhler HR (2009) The impact of environmental chemicals on wildlife vertebrates. Rev Environ Contam Toxicol 198:1–47
Bigatti G, Averbuj A, Braga Castro I, Primost M, Carranza A, Commendatore M, Fillmann G, Delgado E, Scarabino F, del Brío F, Franco M, Letamendía M, Martínez G, Sebastián Sauco S, Penchaszadeh PE (2014) Situación de contaminación en las costas del sur de Brazil, Uruguay y Argentina luego de la prohibición mundial de TBT. In: Goso C (ed) Nuevas miradas a la problemática de los ambientes costeros. Difusión, Relaciones y Actividades Culturales (DIRAC) – Facultad de Ciencias, Montevideo, Uruguay. 277–301
Buggy CJ, Tobin JM (2006) Seasonal and spatial distributions of tributyltin in surface sediment of the Tolka Estuary, Dublin, Ireland. Environ Pollut 143:294–303
Castro IB, Arroyo M, Costa P, Fillmann G (2012) Butyltin compounds and imposex levels in Ecuador. Arch Environ Contam Toxicol 62:68–77
Cazzaniga NJ (1990) Sexual dimorphism in Pomacea canaliculata. Veliger 33:390–394
Claiborne A (1985) Catalase activity. In: Greenwald R (ed) CRC handbook of methods for oxygen radical research. CRC Press, Boca Raton, FL, p 283–284
Couceiro L, Díaz J, Albaina N, Barreiro R, Irabien JA, Ruiz JM (2009) Imposex and gender-independent butyltin accumulation in the gastropod Nassarius reticulatus from the Cantabrian coast (N Atlantic Spain). Chemosphere 76:424–427
Devier MH, Augagneur S, Budzinski H, Mora P, Narbonne JF, Garrigues P (2003) Microcosm tributyltin bioaccumulation and multibiomarker assessment in the blue mussel Mytilus edulis. Environ Toxicol Chem 22:2679–2687
Dickinson DA, Forman HJ (2002) Cellular glutathione and thiols metabolism. Biochem Pharmacol 64:1019–1026
Dowson PH, Bubb JM, LesterJN (1996) Persistence and degradation pathways of tributyltin in freshwater and estuarine sediments. Estuar Coast Shelf S 42:551–562
Ellman GL, Courtney KD, Andres Jr V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95
Fent K (1996) Ecotoxicology of organotin compounds. Crit Rev Toxicol 26:1–117
Fent K, Weston AA, Caminada D (2006) Ecotoxicology of human pharmaceuticals. Aquat Toxicol 73:122–159
Giraud-Billoud M, Vega IA, Wuilloud RG, Clément ME, Castro-Vazquez A (2013) Imposex and novel mechanisms of reproductive failure induced by tributyltin (TBT) in the freshwater snail Pomacea canaliculata. Environ Toxicol Chem 32:2365–2371
GISD: Global Invasive Species Database (2016) http://www.iucngisd.org/gisd/species.php?sc=135. Accessed 22 October 2016.
Hermes-Lima M, Storey JM, Storey KB (1998) Antioxidant defenses and metabolic depression. The hypothesis of preparation for oxidative stress in land snails. Comp Biochem Phys Part B 120:437–448
Higuera-Ruiz R, Elorza J (2011) Shell thickening and chambering in the oyster Crassostrea gigas: natural and anthropogenic influence of tributyltin contamination. Environ Technol 32:583–591
Hoch M (2001) Organotin compounds in the environment-an overview. Appl Geochem 16:719–743
Jagtap JT, Shejule KB, Jaiswal DP (2011) Acute toxicity study of tributyltin chloride on the freshwater bivalve, Lamellidens marginalis. World J Fish Marine Sci 3:100–103
Kim BM, Rhee JS, Park GS, Lee J, Lee YM, Lee JS (2011) Cu/Zn- and Mn-superoxide dismutase (SOD) from the copepod Tigriopus japonicus: Molecular cloning and expression in response to environmental pollutants. Chemosphere 84:1467–1475
Labrot F, Ribera D, Saint Denis M, Narbonne JF (1996) 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. Biomarkers 1:21–28
Láng G, Kufcsák O, Szegletes T, Nemcsók J (1997) Quantitive distributions of different cholinesterases and inhibition of acetylcholinesterase by metidathion and paraquat in alimentary canal of common carp. Gen Pharmac 29:55–59
Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278
Leung K, Grist E, Morley N, Morritt D, Crane M (2007) Chronic toxicity of tributyltin to development and reproduction of the European freshwater snail Lymnaea stagnalis (L.). Chemosphere 66:1358–1366
Liu WH, Chiu YW, Huang DJ, Liu MY, Lee CC, Liu LL (2006) Imposex in the golden apple snail Pomacea canaliculata in Taiwan. Sci Total Environ 371:138–143
Lowry OH, Rosebrough A, Farr L, Randall RS (1951) Protein measurement with the folin phenol reagent. J Biol Chem 249:265–275
Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30
Martins SE, Bianchini A (2011) Toxicity tests aiming to protect Brazilian aquatic systems: current status and implications for management. J Environ Monitor 13:1866–1875
Matthiessen P (2013) Detection, monitoring, and control of tributyltin - an almost complete success story. Environ Toxicol Chem 32:487–489
Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175
Mitra S, Gera R, Siddiquib WA, Khandelwal S (2013) 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. Toxicology 310:39–52
Nakayama K, OshimaY, Tachibana T, Furuse M, Honjo T (2007) Alteration of monoamine concentrations in the brain of medaka, Oryzias latipes, exposed to tributyltin. Environ Toxicol 22:53–57
Pagliarani A, Nesci S, Ventrella V (2013) Toxicity of organotin compounds: shared and unshared biochemical targets and mechanisms in animal cells. Toxicol in Vitro 27:978–990
Paz-Villarraga CA, Castro IB, Miloslavich P, Fillmann G (2015) Venezuelan Caribbean Sea under the threat of TBT. Chemosphere 119:704–710
Pinochet H, Tessini C, Bravo M, Quiroz W, De Gregori I (2009) Butyltin compounds and their relation with organic matter in marine sediments from San Vicente Bay, Chile. Environ Monit Assess 155:341–353
PNA: Prefectura Naval Argentina (1998) Régimen para la protección del medioambiente. Ordenanza No 4/98. Buenos Aires, Argentina
Quintas PY, Oliva AL, Arias A, Domini CE, Alvarez MB, Garrido M, Marcovecchio JE (2016) Seasonal changes in organotin compounds in sediments from the Bahía Blanca Estuary. Environ Earth Sci 75:659–671
Rabitto IS, Alves Costa JRM, Silva de Assis HC, Pelletier É, Akaishi FM, Anjos A, Randi MAF, Oliveira Ribeiroa CA (2005) Effects of dietary Pb(II) and tributyltin on neotropical fish, Hoplias malabaricus: histopathological and biochemical findings. Ecotox Environ Safe 60:147–156
Rand GM (1995) Fundamentals of aquatic toxicology: effects, environmental fate, and risk assessment, 2nd edn. Taylor & Francis, London
Rodríguez Grimón RO, Arroyo Osorio MF, de Freitas DM, Castro IB (2016) Tributyltin impacts in Galapagos Islands and Ecuadorian shore: marine protected areas under threat. Marine Policy 69:24–31
Rüdel H (2003) Case study: bioavailability of tin and tin compounds. Ecotox Environ Safe 56:180–189
Sternberg RM, Gooding MP, Hotchkiss AK, LeBlanc GA (2009) Environmental-endocrine control of reproductive maturation in gastropods: implications for the mechanism of tributyltin induced imposex in prosobranchs. Ecotoxicology 19:4–23
Tallarico LF (2016) Freshwater gastropods as a tool for ecotoxicology assessments in Latin America. Amer Malac Bull 33:330–336
Tessier E, Amouroux D, Morin A, Christian L, Thybaud E, Vindimian E, Donard OFX (2007) Tri)Butyltin biotic degradation rates and pathways in different compartments of a freshwater model ecosystem. Sci Total Environ 388:214–233
Tietze F (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 27:502–522
Tsunoda M, Konno N, Nakano K, Liu Y (2004) Altered metabolism of dopamine in the midbrain of mice treated with tributyltin chloride via subacute oral exposure. Environ Sci 11:209–219
US EPA (2002) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms, 5th edition. EPA-821-R-02-012. United States Environmnental Protecion Agency, Washington, DC, USA.
US EPA (2003) Ambient aquatic life water quality criteria for tributyltin (TBT) – Final. EPA 822-R-03-031. United States Environmnental Protecion Agency, Washington, DC, USA.
Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotox Environ Safe 64:178–189
Waisbaum RG, Rodriguez C, Nudelman NS (2010) Determination of TBT in water and sediment samples along the Argentine Atlantic coast. Environ Technol 31:1335–1342
Wang CG, Chen YX, Li Y, Wei W, Yu Q (2005) Effects of low dose tributyltin on activities of hepatic antioxidant and phase II enzymes in Sebastiscus marmoratus. Bull Environ Contam Toxicol 74:114–119
Wang X, Fang C, Hong H, Wang WX (2010) Gender differences in TBT accumulation and transformation in Thais clavigera after aqueous and dietary exposure. Aquat Toxicol 99:413–422
Wang XH, Hong HS, Zhao DM, Hong LY (2008) Environmental behavior of organotin compounds in the costal environment of Xiamen, China. Mar Poll Bull 57:419–424
Zhou J, Zhu X, Cai Z (2010) Tributyltin toxicity in abalone (Haliotis diversicolor supertexta) assessed by antioxidant enzyme activity, metabolic response, and histopathology. J Hazard Mater 183:428–433
Acknowledgements
The authors are indebted to the Universidad de Buenos Aires and the Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET). MLM acknowledges fellowship from the United Nations Environmental Program-Argentina. The authors also thank to anonymous reviewers for helpful comments on a previous version of the manuscript. This study was funded by grants to the Project N° 02/018/Subproject B-C-53 from the United Nations Environmental Program-Argentina (UNEP-ARG), and N° 20020130100454BA from the Universidad de Buenos Aires.
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Martínez, M.L., Piol, M.N., Sbarbati Nudelman, N. et al. Tributyltin bioaccumulation and toxic effects in freshwater gastropods Pomacea canaliculata after a chronic exposure: field and laboratory studies. Ecotoxicology 26, 691–701 (2017). https://doi.org/10.1007/s10646-017-1801-8
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DOI: https://doi.org/10.1007/s10646-017-1801-8