Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-10T15:44:54.126Z Has data issue: false hasContentIssue false

Oxidative stress indicators in populations of the gastropod Buccinanops globulosus affected by imposex

Published online by Cambridge University Press:  22 December 2015

M. A. Primost
Affiliation:
Instituto de Biología de Organismos Marinos IBIOMAR – CONICET, Bvd. Brown 2915, U9120ACV Puerto Madryn, Chubut, Argentina
S. E. Sabatini*
Affiliation:
IQUIBICEN-Dpto Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pab. II, Intendente Guiraldes 2160, C1428EHA, Ciudad Autónoma de Buenos Aires, Argentina Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pab. II, Intendente Guiraldes 2160, C1428EHA. Ciudad Autónoma de Buenos Aires, Argentina
P. Di Salvatore
Affiliation:
Centro Austral de Investigaciones Científicas (CADIC)-CONICET, Houssay 200, V9410CAB. Ushuaia, Argentina
M. C. Ríos De Molina
Affiliation:
IQUIBICEN-Dpto Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pab. II, Intendente Guiraldes 2160, C1428EHA, Ciudad Autónoma de Buenos Aires, Argentina
G. Bigatti
Affiliation:
Instituto de Biología de Organismos Marinos IBIOMAR – CONICET, Bvd. Brown 2915, U9120ACV Puerto Madryn, Chubut, Argentina Facultad de Ciencias Naturales, Universidad Nacional de la Patagonia San Juan Bosco (UNPSJB), Bvd. Brown S/N; U9120ACV Puerto Madryn, Chubut, Argentina
*
Correspondence should be addressed to:S.E. Sabatini, IQUIBICEN-Dpto Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pab. II, Intendente Guiraldes 2160, C1428EHA, Ciudad Autónoma de Buenos Aires, Argentina email: sabatini@bg.fcen.uba.ar

Abstract

The gastropod Buccinanops globulosus is commonly used as a bioindicator of tributyltin (TBT) contamination due to its high imposex incidence in maritime traffic areas. The aim of this study was to evaluate both oxidative stress in B. globulosus at three sites with different maritime activity, and imposex incidence in Nuevo Gulf, Argentina. Oxidative stress parameters in digestive glands, like superoxide dismutase (SOD) and glutathione-S-transferase (GST) activities, reduced glutathione levels (GSH), and oxidative damage to lipids, estimated as thiobarbituric acid reactive substances (TBARs) as well as imposex parameters (% imposex and female penis length (FPL)) were measured in females. Gastropods from the harbour area showed 100% imposex, the highest FPL and TBARs content, as well as GSH levels and SOD activity.

The different oxidative stress responses and high imposex incidence at the harbour site may indicate a negative effect on the organism's physiological state due to environmental pollution.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Almeida, E.A., Bainy, A.C.D., Dafre, A.L., Gomes, O.F., Medeiros, M.H.G. and Di Mascio, P. (2005) Oxidative stress in digestive gland and gill of the brown mussel (Perna perna) exposed to air and re-submersed. Journal of Experimental Marine Biology and Ecology 318, 2130.Google Scholar
Alzieu, C. (2000) Environmental impact of TBT: the French experience. Science of the Total Environment 258, 99102.CrossRefGoogle ScholarPubMed
An, M.I., An, K.W. and Choi, C.Y. (2009) Changes in antioxidant enzyme activity and physiological responses to cadmium and ributyltin exposure in the ark shell, Scapharca broughtonii . Molecular and Cellular Toxicology 5, 273282.Google Scholar
Anderson, M.E. (1985) Determination of glutathione and glutathione disulfide in biological samples. Methods in Enzymology 113, 548.Google Scholar
Antizar-Ladislao, B. (2008) Environmental levels, toxicity and human exposure to tributyltin (TBT)-contaminated marine environment. A review. Environment International 34, 292308.Google Scholar
APPM (2013) Administración Portuaria de Puerto Madryn. http://www.appm.com.ar/. vol. 2013.Google Scholar
Armstrong, R.N. (1997) Structure, catalytic mechanism, and evolution of the glutathione transferases. Chemical Research in Toxicology 10, 218.CrossRefGoogle ScholarPubMed
Avaca, M.S., Narvarte, M. and Martín, P. (2013) Age, growth and mortality in Buccinanops globulosus (Gastropoda: Nassariidae) from Golfo Nuevo (Argentina). Marine Biology Research 9, 208219.Google Scholar
Averbuj, A., Rocha, M.N. and Zabala, S. (2014) Embryonic development and reproductive seasonality of Buccinanops globulosus (Nassariidae) (Kiener, 1834) in Patagonia, Argentina. Invertebrate Reproduction and Development 58, 138147.Google Scholar
Bainy, A.C.D., Almeida, E.A., Muller, I.C., Ventura, E.C. and Medeiros, I.D. (2000) Biochemical responses in farmed mussel Perna perna transplanted to contaminated sites on Santa Catarina Island, SC, Brazil. Marine Environmental Research 50, 411416.Google Scholar
Beauchamp, C. and Fridovich, I. (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44, 276287.Google Scholar
Belcheva, N., Zakhartsev, M., Dovzhenko, N., Zhukovskaya, A., Kavun, V. and Chelomin, V. (2011) Anthropogenic pollution stimulates oxidative stress in soft tissues of mussel Crenomytilus grayanus (Dunker 1853). Ocean Science Journal 46, 8594.Google Scholar
Bernat, P., Gajewska, E., Szewczyk, R., Słaba, M. and Długoński, J. (2014) Tributyltin (TBT) induces oxidative stress and modifies lipid profile in the filamentous fungus Cunninghamella elegans . Environmental Science and Pollution Research 21, 42284235.Google Scholar
Bigatti, G. and Carranza, A. (2007) Phenotypic variability associated with the occurrence of imposex in Odontocymbiola magellanica from Golfo Nuevo, Patagonia. Journal of the Marine Biological Association of the United Kingdom 87, 755759.Google Scholar
Bigatti, G. and Penchaszadeh, P.E. (2005) Imposex in Odontocymbiola magellanica (Caenogastropoda: Volutidae) in Patagonia. Comunicaciones de la Sociedad Malacológica del Uruguay 9, 371375.Google Scholar
Bigatti, G., Primost, M.A., Cledón, M., Averbuj, A., Theobald, N., Gerwinski, W., Arntz, W., Morriconi, E. and Penchaszadeh, P.E. (2009) Biomonitoring of TBT contamination and imposex incidence along 4700 km of Argentinean shoreline (SW Atlantic: From 38S to 54S). Marine Pollution Bulletin 58, 695701.Google Scholar
Bökenhans, V. (2014) Estimación de la edad y crecimiento de dos poblaciones de Buccinanops globulosus del Golfo Nuevo . Degree thesis. Universidad Nacional de la Patagonia San Juan Bosco, Puerto Madryn.Google Scholar
Borković, S.S., Šaponjić, J.S., Pavlović, S.Z., Blagojević, D.P., Milošević, S.M., Kovačević, T.B., Radojičić, R.M., Spasić, M.B., Žikić, R.V. and Saičić, Z.S. (2005) The activity of antioxidant defence enzymes in the mussel Mytilus galloprovincialis from the Adriatic Sea. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 141, 366374.Google Scholar
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254.Google Scholar
Brown, R.J., Galloway, T.S., Lowe, D., Browne, M.A., Dissanayake, A., Jones, M.B. and Depledge, M.H. (2004) Differential sensitivity of three marine invertebrates to copper assessed using multiple biomarkers. Aquatic Toxicology 66, 267278.Google Scholar
Clarke, K.R. and Gorley, R.N. (2006) Change in marine communities: an approach to statistical analysis and interpretation. PRIMER v6: User Manual/Tutorial. Plymouth: PRIMER-E, 192 pp.Google Scholar
Chagot, D., Alzieu, C., Sanjuan, J. and Grizel, H. (1990) Sublethal and histopathological effects of trace levels of tributyltin fluoride on adult oysters Crassostrea gigas . Aquatic Living Resources 3, 121130.Google Scholar
Chandran, R., Sivakumar, A.A., Mohandass, S. and Aruchami, M. (2005) Effect of cadmium and zinc on antioxidant enzyme activity in the gastropod, Achatina fulica . Comparative Biochemistry and Physiology, Part C: Toxicology and Pharmacology 140, 422426.Google Scholar
Chen, H.G., Jia, X.P., Cai, W.G., Lin, Q. and Ma, S.W. (2011) Antioxidant responses and bioaccumulation in green-lipped mussels (Perna viridis) under acute tributyltin chloride exposure. Bulletin of Environmental Contamination and Toxicology 87, 506511.Google Scholar
Cheung, C.C.C., Zheng, G.J., Li, A.M.Y., Richardson, B.J. and Lam, P.K.S. (2001) Relationships between tissue concentrations of polycyclic aromatic hydrocarbons and antioxidative responses of marine mussels Perna viridis. Aquatic Toxicology 52, 189203.Google Scholar
Commendatore, M.G. and Esteves, J.L. (2007) An assessment of oil pollution in the coastal zone of Patagonia, Argentina. Environmental Management 40, 814821.Google Scholar
Commendatore, M.G., Esteves, J.L. and Colombo, J.C. (2000) Hydrocarbons in coastal sediments of Patagonia, Argentina: levels and probable sources. Marine Pollution Bulletin 40, 989998.CrossRefGoogle Scholar
Dahlhoff, E.P. (2004) Biochemical indicators of stress and metabolism: applications for marine ecological studies. Annual Review of Physiology 66, 183207.Google Scholar
Davies, K.J.A. (1995) Oxidative stress: the paradox of aerobic life. Biochemical Society Symposia 61, 132.Google Scholar
de Almeida, E.A., Miyamoto, S., Bainy, A.C.D., de Medeiros, M.H.G. and Di Mascio, P. (2004) Protective effect of phospholipid hydroperoxide glutathione peroxidase (PHGPx) against lipid peroxidation in mussels Perna perna exposed to different metals. Marine Pollution Bulletin 49, 386392.Google Scholar
del Brio, F., Castro, I.B., Fillmann, G., Commendatore, M., Gomes Costa, P. and Bigatti, G. (in press) Distribution and bioaccumulation of butyltins in the edible gastropod Odontocymbiola magellanica. Marine Biology Research.Google Scholar
Di Salvatore, P., Calcagno, J.A., Ortíz, N., Ríos de Molina, M.C. and Sabatini, S.E. (2013) Effect of seasonality on oxidative stress responses and metal accumulation in soft tissues of Aulacomya atra, a mussel from the South Atlantic Patagonian coast. Marine Environmental Research 92, 244252.CrossRefGoogle Scholar
Doyen, P., Vasseur, P. and Rodius, F. (2005) cDNA cloning and expression pattern of pi-class glutathione-S-transferase in the fresh water bivalves Uniotumidus and Corbicula fluminea . Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 140, 300308.Google Scholar
Esteves, J.L., Commendatore, M., Nievas, M.L., Massara Paletto, V. and Amín, O. (2006) Hydrocarbon pollution in coastal sediments of Tierra del Fuego Islands, Patagonia Argentina. Marine Pollution Bulletin 52, 582590.Google Scholar
Giarratano, E., Duarte, C.A. and Amin, O.A. (2010) Biomarkers and heavy metal bioaccumulation in mussels transplanted to coastal waters of the Beagle Channel. Ecotoxicology and Environmental Safety 73, 270279.Google Scholar
Giarratano, E., Gil, M.N. and Malanga, G. (2013) Assessment of antioxidant responses and trace metal accumulation by digestive gland of ribbed mussel Aulacomya atra atra from Northern Patagonia. Ecotoxicology and Environmental Safety 92, 3950.Google Scholar
Gibbs, P.E. and Bryan, G.W. (1986) Reproductive failure in populations of the dog-whelk, Nucella lapillus, caused by imposex induced by tributyltin from antifouling paints. Journal of the Marine Biological Association of the United Kingdom 66, 767777.Google Scholar
Gil, M.N., Harvey, M. and Esteves, J.L. (1988) Metal content in bivalves molluscs from the San Jose and Nuevo gulfs, Patagonia Argentina. Marine Pollution Bulletin 19, 181182.Google Scholar
Gil, M.N., Harvey, M.A. and Esteves, J.L. (1999) Heavy metals in intertidal surface sediments from the Patagonian Coast, Argentina. Bulletin of Environmental Contamination and Toxicology 63, 5258.Google Scholar
Gil, M.N., Torres, A., Harvey, M. and Esteves, J.L. (2006) Metales pesados en organismos marinos de la zona costera de la Patagonia argentina continental. Revista de Biologia Marina y Oceanografia 41, 167176.Google Scholar
Gopalakrishnan, S., Huang, W.B., Wang, Q.W., Wu, M.L., Liu, J. and Wang, K.J. (2011) Effects of tributyltin and benzo[a]pyrene on the immune-associated activities of hemocytes and recovery responses in the gastropod abalone, Haliotis diversicolor . Comparative Biochemistry and Physiology, Part C: Toxicology and Pharmacology 154, 120128.Google Scholar
Habig, W.H., Pabst, M.J. and Jakoby, W.B. (1974) Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry 249, 71307139.Google Scholar
Hayes, J.D., Flanagan, J.U. and Jowsey, I.R. (2005) Glutathione transferases. Annual Review of Pharmacology and Toxicology 45, 5188.Google Scholar
Huang, Z., Chen, Y., Zhao, Y., Zuo, Z., Chen, M. and Wang, C. (2005) Antioxidant responses in Meretrix meretrix exposed to environmentally relevant doses of tributyltin. Environmental Toxicology and Pharmacology 20, 107111.Google Scholar
Jia, X., Zhang, Z., Wang, S., Lin, P., Zou, Z., Huang, B. and Wang, Y. (2009) Effects of tributyltin (TBT) on enzyme activity and oxidative stress in hepatopancreas and hemolymph of small abalone, Haliotis diversicolor supertexta . Chinese Journal of Oceanology and Limnology 27, 816824.Google Scholar
Karakoc, F.T., Hewer, A., Phillips, D.H., Gaines, A.F. and Yuregir, G. (1997) Biomarkers of marine pollution observed in species of mullet living in two eastern Mediterranean harbours. Biomarkers 2, 303309.Google Scholar
Kim, S.K., Oh, J.R., Shim, W.J., Lee, D.H., Yim, U.H., Hong, S.H., Shin, Y.B. and Lee, D.S. (2002) Geographical distribution and accumulation features of organochlorine residues in bivalves from coastal areas of South Korea. Marine Pollution Bulletin 45, 268279.Google Scholar
Leonard, S.S., Harris, G.K. and Shi, X. (2004) Metal-induced oxidative stress and signal transduction. Free Radical Biology and Medicine 37, 19211942.Google Scholar
Liu, H.G., Wang, Y., Lian, L. and Xu, L.H. (2006) Tributyltin induces DNA damage as well as oxidative damage in rats. Environmental Toxicology 21, 166171.Google Scholar
Livingstone, D.R. (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Marine Pollution Bulletin 42, 656666.Google Scholar
Malanga, G., Estevez, M.S., Calvo, J. and Puntarulo, S. (2004) Oxidative stress in limpets exposed to different environmental conditions in the Beagle Channel. Aquatic Toxicology 69, 299309.Google Scholar
Márquez, F., González, R.J. and Bigatti, G. (2011) Combined methods to detect pollution effects on shell shape and structure in Neogastropods. Ecological Indicators 11, 248254.Google Scholar
Massara Paletto, V., Commendatore, M.G. and Esteves, J.L. (2008) Hydrocarbon levels in sediments and bivalve mollusks from Bahía Nueva (Patagonia, Argentina): an assessment of probable origin and bioaccumulation factors. Marine Pollution Bulletin 56, 20822105.Google Scholar
Meador, J.P., Stein, J.E., Reichert, W.L. and Varanasi, U. (1995) Bioaccumulation of polycyclic aromatic hydrocarbons by marine organisms. In Ware, G.W. (ed.) Reviews of environmental contamination and toxicology. New York, NY: Springer, Volume 143, pp. 79165.Google Scholar
Narvarte, M.A., Willers, V., Avaca, M.S. and Echave, M.E. (2008) Population structure of the snail Buccinanops globulosum (Prosobranchia, Nassariidae) in San Matías Gulf, Patagonia Argentina: isolated enclaves? Journal of Sea Research 60, 144150.Google Scholar
Nicholson, S. and Lam, P.K.S. (2005) Pollution monitoring in Southeast Asia using biomarkers in the mytilid mussel Perna viridis (Mytilidae: Bivalvia). Environment International 31, 121132.Google Scholar
Nishikawa, J., Mamiya, S., Kanayama, T., Nishikawa, T., Shiraishi, F. and Horiguchi, T. (2004) Involvement of the retinoid x receptor in the development of imposex caused by organotins in gastropods. Environmental Science and Technology 38, 62716276.CrossRefGoogle ScholarPubMed
Pastorino, G. (1993) The taxonomic status of Buccinanops d'Orbigny, 1841 (Gastropoda: Nassariidae). The Veliger 36, 160165.Google Scholar
Penchaszadeh, P.E. (1971) Aspectos de la embriogenesis de algunos gasterópodos del genero Buccinanops d'Orbigny, 1841 (Gastropoda, Prosobranchiata, Buccinidae). Physis 30, 475482.Google Scholar
Primost, M.A. (2014) Ecotoxicología y alteraciones morfo-funcionales en gasterópodos marinos expuestos a contaminación por organometales y metales . PhD thesis. Universidad Nacional de La Plata, Argentina.Google Scholar
Primost, M.A., Bigatti, G. and Márquez, F. (in press). Shell shape variation as indicator of harbour pollution in marine gastropods affected by imposex. Marine and Freshwater Research.Google Scholar
Prohaska, J.R. (1980) The glutathione peroxidase activity of glutathione S-transferases. Biochimica et Biophysica Acta – Enzymology 611, 8798.Google Scholar
Regoli, F. and Principato, G. (1995) Glutathione, glutathione-dependent and antioxidant enzymes in mussel, Mytilus galloprovincialis, exposed to metals under field and laboratory conditions: implications for the use of biochemical biomarkers. Aquatic Toxicology 31, 143164.Google Scholar
Sabatini, S.E., Rocchetta, I., Luquet, C.M., Guido, M.I. and Ríos de Molina, M.C. (2009) Dietary copper effects in the estuarine crab, Neohelice (Chasmagnathus) granulata, maintained at two different salinities. Comparative Biochemistry and Physiology, Part C 150, 521527.Google Scholar
Sabatini, S.E., Rocchetta, I., Luquet, C.M., Guido, M.I. and Ríos de Molina, M.C. (2011a) Effects of sewage pollution and bacterial load on growth and oxidative balance in the freshwater mussel Diplodon chilensis . Limnologica 41, 356362.Google Scholar
Sabatini, S.E., Rocchetta, I., Nahabedian, D.E., Luquet, C.M., Eppis, M.R., Bianchi, L. and Ríos de Molina, M.C. (2011b) Oxidative stress and histological alterations produced by dietary copper in the fresh water bivalve Diplodon chilensis . Comparative Biochemistry and Physiology, Part C 154, 391398.Google Scholar
Sayeed, I., Parvez, S., Pandey, S., Bin-Hafeez, B., Haque, R. and Raisuddin, S. (2003) Oxidative stress biomarkers of exposure to deltamethrin in freshwater fish, Channa punctatus Bloch. Ecotoxicology and Environmental Safety 56, 295301.Google Scholar
Scarabino, V. (1977) Moluscos del Golfo San Matías, provincia de Río Negro, República Argentina. Inventario y claves para su identificación. Comisión de la Sociedad Malacológica de Uruguay 4, 177285.Google Scholar
Sheehan, D. and Power, A. (1999) Effects of seasonality on xenobiotic and antioxidant defence mechanisms of bivalve molluscs. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology 123, 193199.Google Scholar
Sokal, R.R. and Rohlf, F.J. (1979) Introducción a la bioestadística. Barcelona, España: Reverté.Google Scholar
Torres, P.J., Commendatore, M.G., Primost, M.A. and Bigatti, G. (2013) Hidrocarburos Poliaromáticos (PAHs) en Buccinanops globulosus afectados por imposex. Proceedings of the Abstract book I Congreso Argentino de Malacología (CAM), 99 pp.Google Scholar
Valavanidis, A., Vlahogianni, T., Dassenakis, M. and Scoullos, M. (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicology and Environmental Safety 64, 178189.Google Scholar
Vavilin, D.V., Ducruet, J.M., Matorin, D.N., Venediktov, P.S. and Rubin, A.B. (1998) Membrane lipid peroxidation, cell viability and photosystem II activity in the green alga Chlorella pyrenoidosa subjected to various stress conditions. Journal of Photochemistry and Photobiology, B: Biology 42, 233239.Google Scholar
Viarengo, A., Canesi, L., Pertica, M. and Livingstone, D.R. (1991) Seasonal variations in the antioxidant defence systems and lipid peroxidation of the digestive gland of mussels. Comparative Biochemistry and Physiology, Part C: Comparative Pharmacology 100, 187190.Google Scholar
Viarengo, A., Canesi, L., Pertica, M., Poli, G., Moore, M.N. and Orunesu, M. (1990) Heavy metal effects on lipid peroxidation in the tissues of Mytilus galloprovincialis Lam. Comparative Biochemistry and Physiology, Part C: Comparative Pharmacology 97, 3742.Google Scholar
Wang, C.G., Chen, Y.X., Li, Y., Wei, W. and Yu, Q. (2005) Effects of low dose tributyltin on activities of hepatic antioxidant and phase II enzymes in Sebastiscus marmoratus . Bulletin of Environmental Contamination and Toxicology 74, 114119.Google Scholar
Wang, L., Yan, B., Liu, N., Li, Y. and Wang, Q. (2008) Effects of cadmium on glutathione synthesis in hepatopancreas of freshwater crab, Sinopotamon yangtsekiense . Chemosphere 74, 5156.Google Scholar
Winston, G.W. and Di Giulio, R.T. (1991) Prooxidant and antioxidant mechanisms in aquatic organisms. Aquatic Toxicology 19, 137161.Google Scholar
Young, I. and Woodside, J. (2001) Antioxidants in health and disease. Journal of Clinical Pathology 54, 176186.Google Scholar
Zhou, J., Zhu, X. and Cai, Z. (2010) Tributyltin toxicity in abalone (Haliotis diversicolor supertexta) assessed by antioxidant enzyme activity, metabolic response, and histopathology. Journal of Hazardous Materials 183, 428433.CrossRefGoogle ScholarPubMed