Artículo

Primost, M.A.; Sabatini, S.E.; Di Salvatore, P.; Ríos De Molina, M.C.; Bigatti, G. "Oxidative stress indicators in populations of the gastropod Buccinanops globulosus affected by imposex" (2017) Journal of the Marine Biological Association of the United Kingdom. 97(1):35-42
El editor solo permite decargar el artículo en su versión post-print desde el repositorio. Por favor, si usted posee dicha versión, enviela a
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

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. Copyright © Marine Biological Association of the United Kingdom 2015.

Registro:

Documento: Artículo
Título:Oxidative stress indicators in populations of the gastropod Buccinanops globulosus affected by imposex
Autor:Primost, M.A.; Sabatini, S.E.; Di Salvatore, P.; Ríos De Molina, M.C.; Bigatti, G.
Filiación:Instituto de Biologiá de Organismos Marinos IBIOMAR - CONICET, Bvd. Brown 2915, Puerto Madryn, Chubut, U9120ACV, Argentina
IQUIBICEN-Dpto Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pab. II, Intendente Guiraldes 2160, Ciudad Autónoma de Buenos Aires, C1428EHA, Argentina
Departamento de Biodiversidad y Biologiá Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pab. II, Intendente Guiraldes 2160, Ciudad Autónoma de Buenos Aires, C1428EHA, Argentina
Centro Austral de Investigaciones Científicas (CADIC)-CONICET, Houssay 200, Ushuaia, V9410CAB, Argentina
Facultad de Ciencias Naturales, Universidad Nacional de la Patagonia San Juan Bosco (UNPSJB), Bvd. Brown S/N U9120ACV, Puerto Madryn, Chubut, Argentina
Palabras clave:Buccinanops globulosus; imposex; marine pollution; Nassariidae; Oxidative stress; bioindicator; chemical pollutant; environmental fate; enzyme activity; harbor; imposex; marine pollution; oxidative stress; pollution effect; snail; tributyltin; Argentina; Atlantic Ocean; Nuevo Gulf; Gastropoda; Nassariidae
Año:2017
Volumen:97
Número:1
Página de inicio:35
Página de fin:42
DOI: http://dx.doi.org/10.1017/S0025315415002155
Título revista:Journal of the Marine Biological Association of the United Kingdom
Título revista abreviado:J. Mar. Biol. Assoc. U.K.
ISSN:00253154
CODEN:JMBAA
Registro:http://digital.bl.fcen.uba.ar/collection/paper/document/paper_00253154_v97_n1_p35_Primost

Referencias:

  • Almeida, E.A., Bainy, A.C.D., Dafre, A.L., Gomes, O.F., Medeiros, M.H.G., Di Mascio, P., Oxidative stress in digestive gland and gill of the brown mussel (Perna perna) exposed to air and re-submersed (2005) Journal of Experimental Marine Biology and Ecology, 318, pp. 21-30
  • Alzieu, C., Environmental impact of TBT: The French experience (2000) Science of the Total Environment, 258, pp. 99-102
  • An, M.I., An, K.W., Choi, C.Y., Changes in antioxidant enzyme activity and physiological responses to cadmium and ributyltin exposure in the ark shell, Scapharca broughtonii (2009) Molecular and Cellular Toxicology, 5, pp. 273-282
  • Anderson, M.E., Determination of glutathione and glutathione disulfide in biological samples (1985) Methods in Enzymology, 113, p. 548
  • Antizar-Ladislao, B., Environmental levels, toxicity and human exposure to tributyltin (TBT)-contaminated marine environment (2008) A Review. Environment International, 34, pp. 292-308
  • (2013) Administración Portuaria de Puerto Madryn, , http://www.appm.com.ar/.2013
  • Armstrong, R.N., Structure, catalytic mechanism, and evolution of the glutathione transferases (1997) Chemical Research in Toxicology, 10, pp. 2-18
  • Avaca, M.S., Narvarte, M., Martín, P., Age, growth and mortality in Buccinanops globulosus (Gastropoda: Nassariidae) from Golfo Nuevo (Argentina) (2013) Marine Biology Research, 9, pp. 208-219
  • Averbuj, A., Rocha, M.N., Zabala, S., Embryonic development and reproductive seasonality of Buccinanops globulosus (Nassariidae) (Kiener, 1834) in Patagonia, Argentina (2014) Invertebrate Reproduction and Development, 58, pp. 138-147
  • Bainy, A.C.D., Almeida, E.A., Muller, I.C., Ventura, E.C., Medeiros, I.D., Biochemical responses in farmed mussel Perna perna transplanted to contaminated sites on Santa Catarina Island, SC, Brazil (2000) Marine Environmental Research, 50, pp. 411-416
  • Beauchamp, C., Fridovich, I., Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels (1971) Analytical Biochemistry, 44, pp. 276-287
  • Belcheva, N., Zakhartsev, M., Dovzhenko, N., Zhukovskaya, A., Kavun, V., Chelomin, V., Anthropogenic pollution stimulates oxidative stress in soft tissues of mussel Crenomytilus grayanus (Dunker 1853) (2011) Ocean Science Journal, 46, pp. 85-94
  • Bernat, P., Gajewska, E., Szewczyk, R., Saba, M., Dugonski, J., Tributyltin (TBT) induces oxidative stress and modifies lipid profile in the filamentous fungus Cunninghamella elegans (2014) Environmental Science and Pollution Research, 21, pp. 4228-4235
  • Bigatti, G., Carranza, A., Phenotypic variability associated with the occurrence of imposex in Odontocymbiola magellanica from Golfo Nuevo, Patagonia (2007) Journal of the Marine Biological Association of the United Kingdom, 87, pp. 755-759
  • Bigatti, G., Penchaszadeh, P.E., Imposex in Odontocymbiola magellanica (Caenogastropoda: Volutidae) in Patagonia (2005) Comunicaciones de la Sociedad Malacológica Del Uruguay, 9, pp. 371-375
  • Bigatti, G., Primost, M.A., Cledón, M., Averbuj, A., Theobald, N., Gerwinski, W., Arntz, W., Penchaszadeh, P.E., Biomonitoring of TBT contamination and imposex incidence along 4700 km of Argentinean shoreline (SW Atlantic: From 38S to 54S) (2009) Marine Pollution Bulletin, 58, pp. 695-701
  • 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
  • Borkovic, S.S., Saponjic, J.S., Pavlovic, S.Z., Blagojevic, D.P., Milosevic, S.M., Kovacevic, T.B., Radojicic, R.M., Saicic, Z.S., The activity of antioxidant defence enzymes in the mussel mytilus galloprovincialis from the adriatic sea (2005) Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, 141, pp. 366-374
  • Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding (1976) Analytical Biochemistry, 72, pp. 248-254
  • Brown, R.J., Galloway, T.S., Lowe, D., Browne, M.A., Dissanayake, A., Jones, M.B., Depledge, M.H., Differential sensitivity of three marine invertebrates to copper assessed using multiple biomarkers (2004) Aquatic Toxicology, 66, pp. 267-278
  • Clarke, K.R., Gorley, R.N., Change in marine communities: An approach to statistical analysis and interpretation (2006) PRIMER v6: User Manual/Tutorial, 192p. , Plymouth: PRIMER-E
  • Chagot, D., Alzieu, C., Sanjuan, J., Grizel, H., Sublethal and histopathological effects of trace levels of tributyltin fluoride on adult oysters Crassostrea gigas (1990) Aquatic Living Resources, 3, pp. 121-130
  • Chandran, R., Sivakumar, A.A., Mohandass, S., Aruchami, M., Effect of cadmium and zinc on antioxidant enzyme activity in the gastropod, Achatina fulica (2005) Comparative Biochemistry and Physiology, Part C: Toxicology and Pharmacology, 140, pp. 422-426
  • Chen, H.G., Jia, X.P., Cai, W.G., Lin, Q., Ma, S.W., Antioxidant responses and bioaccumulation in green-lipped mussels (Perna viridis) under acute tributyltin chloride exposure (2011) Bulletin of Environmental Contamination and Toxicology, 87, pp. 506-511
  • Cheung, C.C.C., Zheng, G.J., Li, A.M.Y., Richardson, B.J., Lam, P.K.S., Relationships between tissue concentrations of polycyclic aromatic hydrocarbons and antioxidative responses of marine mussels Perna viridis (2001) Aquatic Toxicology, 52, pp. 189-203
  • Commendatore, M.G., Esteves, J.L., An assessment of oil pollution in the coastal zone of Patagonia, Argentina (2007) Environmental Management, 40, pp. 814-821
  • Commendatore, M.G., Esteves, J.L., Colombo, J.C., Hydrocarbons in coastal sediments of Patagonia, Argentina: Levels and probable sources (2000) Marine Pollution Bulletin, 40, pp. 989-998
  • Dahlhoff, E.P., Biochemical indicators of stress and metabolism: Applications for marine ecological studies (2004) Annual Review of Physiology, 66, pp. 183-207
  • Davies, K.J.A., Oxidative stress: The paradox of aerobic life (1995) Biochemical Society Symposia, 61, pp. 1-32
  • De Almeida, E.A., Miyamoto, S., Bainy, A.C.D., De Medeiros, M.H.G., Di Mascio, P., Protective effect of phospholipid hydroperoxide glutathione peroxidase (PHGPx) against lipid peroxidation in mussels Perna perna exposed to different metals (2004) Marine Pollution Bulletin, 49, pp. 386-392
  • Del Brio, F., Castro, I.B., Fillmann, G., Commendatore, M., Gomes Costa, P., Bigatti, G., Distribution and bioaccumulation of butyltins in the edible gastropod Odontocymbiola magellanica Marine Biology Research, , in press
  • Di Salvatore, P., Calcagno, J.A., Ortíz, N., Riós De Molina, M.C., Sabatini, S.E., Effect of seasonality on oxidative stress responses and metal accumulation in soft tissues of Aulacomya atra, a mussel from the South Atlantic Patagonian coast (2013) Marine Environmental Research, 92, pp. 244-252
  • Doyen, P., Vasseur, P., Rodius, F., CDNA cloning and expression pattern of pi-class glutathione-S-transferase in the fresh water bivalves Uniotumidus and Corbicula fluminea (2005) Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, 140, pp. 300-308
  • Esteves, J.L., Commendatore, M., Nievas, M.L., Massara Paletto, V., Amín, O., Hydrocarbon pollution in coastal sediments of Tierra del Fuego Islands, Patagonia Argentina (2006) Marine Pollution Bulletin, 52, pp. 582-590
  • Giarratano, E., Duarte, C.A., Amin, O.A., Biomarkers and heavy metal bioaccumulation in mussels transplanted to coastal waters of the Beagle Channel (2010) Ecotoxicology and Environmental Safety, 73, pp. 270-279
  • Giarratano, E., Gil, M.N., Malanga, G., Assessment of antioxidant responses and trace metal accumulation by digestive gland of ribbed mussel Aulacomya atra atra from Northern Patagonia (2013) Ecotoxicology and Environmental Safety, 92, pp. 39-50
  • Gibbs, P.E., Bryan, G.W., Reproductive failure in populations of the dog-whelk, Nucella lapillus, caused by imposex induced by tributyltin from antifouling paints (1986) Journal of the Marine Biological Association of the United Kingdom, 66, pp. 767-777
  • Gil, M.N., Harvey, M., Esteves, J.L., Metal content in bivalves molluscs from the San Jose and Nuevo gulfs, Patagonia Argentina (1988) Marine Pollution Bulletin, 19, pp. 181-182
  • Gil, M.N., Harvey, M.A., Esteves, J.L., Heavy metals in intertidal surface sediments from the Patagonian Coast, Argentina (1999) Bulletin of Environmental Contamination and Toxicology, 63, pp. 52-58
  • Gil, M.N., Torres, A., Harvey, M., Esteves, J.L., Metales pesados en organismos marinos de la zona costera de la Patagonia Argentina continental (2006) Revista de Biologia Marina y Oceanografia, 41, pp. 167-176
  • Gopalakrishnan, S., Huang, W.B., Wang, Q.W., Wu, M.L., Liu, J., Wang, K.J., Effects of tributyltin and benzo[a]pyrene on the immune-associated activities of hemocytes and recovery responses in the gastropod abalone, Haliotis diversicolor (2011) Comparative Biochemistry and Physiology, Part C: Toxicology and Pharmacology, 154, pp. 120-128
  • Habig, W.H., Pabst, M.J., Jakoby, W.B., Glutathione S-transferases: The first enzymatic step in mercapturic acid formation (1974) Journal of Biological Chemistry, 249, pp. 7130-7139
  • Hayes, J.D., Flanagan, J.U., Jowsey, I.R., Glutathione transferases (2005) Annual Review of Pharmacology and Toxicology, 45, pp. 51-88
  • Huang, Z., Chen, Y., Zhao, Y., Zuo, Z., Chen, M., Wang, C., Antioxidant responses in Meretrix meretrix exposed to environmentally relevant doses of tributyltin (2005) Environmental Toxicology and Pharmacology, 20, pp. 107-111
  • Jia, X., Zhang, Z., Wang, S., Lin, P., Zou, Z., Huang, B., Wang, Y., Effects of tributyltin (TBT) on enzyme activity and oxidative stress in hepatopancreas and hemolymph of small abalone, Haliotis diversicolor supertexta (2009) Chinese Journal of Oceanology and Limnology, 27, pp. 816-824
  • Karakoc, F.T., Hewer, A., Phillips, D.H., Gaines, A.F., Yuregir, G., Biomarkers of marine pollution observed in species of mullet living in two eastern Mediterranean harbours (1997) Biomarkers, 2, pp. 303-309
  • Kim, S.K., Oh, J.R., Shim, W.J., Lee, D.H., Yim, U.H., Hong, S.H., Shin, Y.B., Lee, D.S., Geographical distribution and accumulation features of organochlorine residues in bivalves from coastal areas of South Korea (2002) Marine Pollution Bulletin, 45, pp. 268-279
  • Leonard, S.S., Harris, G.K., Shi, X., Metal-induced oxidative stress and signal transduction (2004) Free Radical Biology and Medicine, 37, pp. 1921-1942
  • Liu, H.G., Wang, Y., Lian, L., Xu, L.H., Tributyltin induces DNA damage as well as oxidative damage in rats (2006) Environmental Toxicology, 21, pp. 166-171
  • Livingstone, D.R., Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms (2001) Marine Pollution Bulletin, 42, pp. 656-666
  • Malanga, G., Estevez, M.S., Calvo, J., Puntarulo, S., Oxidative stress in limpets exposed to different environmental conditions in the Beagle Channel (2004) Aquatic Toxicology, 69, pp. 299-309
  • Márquez, F., González, R.J., Bigatti, G., Combined methods to detect pollution effects on shell shape and structure in Neogastropods (2011) Ecological Indicators, 11, pp. 248-254
  • Massara Paletto, V., Commendatore, M.G., Esteves, J.L., Hydrocarbon levels in sediments and bivalve mollusks from Bahiá Nueva (Patagonia, Argentina): An assessment of probable origin and bioaccumulation factors (2008) Marine Pollution Bulletin, 56, pp. 2082-2105
  • Meador, J.P., Stein, J.E., Reichert, W.L., Varanasi, U., Bioaccumulation of polycyclic aromatic hydrocarbons by marine organisms (1995) Reviews of Environmental Contamination and Toxicology, 143, pp. 79-165. , Ware G. W. (ed.) . New York, NY: Springer, Volume
  • Narvarte, M.A., Willers, V., Avaca, M.S., Echave, M.E., Population structure of the snail Buccinanops globulosum (Prosobranchia, Nassariidae) in San Matiás Gulf, Patagonia Argentina: Isolated enclaves (2008) Journal of Sea Research, 60, pp. 144-150
  • Nicholson, S., Lam, P.K.S., Pollution monitoring in Southeast Asia using biomarkers in the mytilid mussel Perna viridis (Mytilidae: Bivalvia) (2005) Environment International, 31, pp. 121-132
  • Nishikawa, J., Mamiya, S., Kanayama, T., Nishikawa, T., Shiraishi, F., Horiguchi, T., Involvement of the retinoid x receptor in the development of imposex caused by organotins in gastropods (2004) Environmental Science and Technology, 38, pp. 6271-6276
  • Pastorino, G., The taxonomic status of Buccinanops d'Orbigny, 1841 (Gastropoda: Nassariidae) (1993) The Veliger, 36, pp. 160-165
  • Penchaszadeh, P.E., Aspectos de la embriogenesis de algunos gasterópodos del genero Buccinanops d'Orbigny, 1841 (Gastropoda, Prosobranchiata, Buccinidae) (1971) Physis, 30, pp. 475-482
  • Primost, M.A., Ecotoxicologiá y alteraciones morfo-funcionales en gasterópodos marinos expuestos a contaminación por organometales y metales (2014) PhD Thesis. Universidad Nacional de la Plata, Argentina
  • Primost, M.A., Bigatti, G., Márquez, F., Shell shape variation as indicator of harbour pollution in marine gastropods affected by imposex Marine and Freshwater Research, , in press
  • Prohaska, J.R., The glutathione peroxidase activity of glutathione S-transferases (1980) Biochimica et Biophysica Acta-Enzymology, 611, pp. 87-98
  • Regoli, F., Principato, G., 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 (1995) Aquatic Toxicology, 31, pp. 143-164
  • Sabatini, S.E., Rocchetta, I., Luquet, C.M., Guido, M.I., Riós De Molina, M.C., Dietary copper effects in the estuarine crab, Neohelice (Chasmagnathus) granulata, maintained at two different salinities (2009) Comparative Biochemistry and Physiology, Part C, 150, pp. 521-527
  • Sabatini, S.E., Rocchetta, I., Luquet, C.M., Guido, M.I., Riós De Molina, M.C., Effects of sewage pollution and bacterial load on growth and oxidative balance in the freshwater mussel Diplodon chilensis (2011) Limnologica, 41, pp. 356-362
  • Sabatini, S.E., Rocchetta, I., Nahabedian, D.E., Luquet, C.M., Eppis, M.R., Bianchi, L., Riós De Molina, M.C., Oxidative stress and histological alterations produced by dietary copper in the fresh water bivalve Diplodon chilensis (2011) Comparative Biochemistry and Physiology, Part C, 154, pp. 391-398
  • Sayeed, I., Parvez, S., Pandey, S., Bin-Hafeez, B., Haque, R., Raisuddin, S., Oxidative stress biomarkers of exposure to deltamethrin in freshwater fish, Channa punctatus Bloch (2003) Ecotoxicology and Environmental Safety, 56, pp. 295-301
  • Scarabino, V., Moluscos del Golfo San Matiás, provincia de Rió Negro, República Argentina (1977) Inventario y Claves para Su Identificación. Comisión de la Sociedad Malacológica de Uruguay, 4, pp. 177-285
  • Sheehan, D., Power, A., Effects of seasonality on xenobiotic and antioxidant defence mechanisms of bivalve molluscs (1999) Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology, 123, pp. 193-199
  • Sokal, R.R., Rohlf, F.J., Introducción a la bioestadística (1979) Barcelona, Espanã: Reverté
  • Torres, P.J., Commendatore, M.G., Primost, M.A., Bigatti, G., Hidrocarburos Poliaromáticos (PAHs) en Buccinanops globulosus afectados por imposex (2013) Proceedings of the Abstract Book i Congreso Argentino de Malacologiá (CAM), 99p
  • Valavanidis, A., Vlahogianni, T., Dassenakis, M., Scoullos, M., Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants (2006) Ecotoxicology and Environmental Safety, 64, pp. 178-189
  • Vavilin, D.V., Ducruet, J.M., Matorin, D.N., Venediktov, P.S., Rubin, A.B., Membrane lipid peroxidation, cell viability and photosystem II activity in the green alga Chlorella pyrenoidosa subjected to various stress conditions (1998) Journal of Photochemistry and Photobiology, B: Biology, 42, pp. 233-239
  • Viarengo, A., Canesi, L., Pertica, M., Livingstone, D.R., Seasonal variations in the antioxidant defence systems and lipid peroxidation of the digestive gland of mussels (1991) Comparative Biochemistry and Physiology, Part C: Comparative Pharmacology, 100, pp. 187-190
  • Viarengo, A., Canesi, L., Pertica, M., Poli, G., Moore, M.N., Orunesu, M., Heavy metal effects on lipid peroxidation in the tissues of Mytilus galloprovincialis Lam (1990) Comparative Biochemistry and Physiology, Part C: Comparative Pharmacology, 97, pp. 37-42
  • 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) Bulletin of Environmental Contamination and Toxicology, 74, pp. 114-119
  • Wang, L., Yan, B., Liu, N., Li, Y., Wang, Q., Effects of cadmium on glutathione synthesis in hepatopancreas of freshwater crab, Sinopotamon yangtsekiense (2008) Chemosphere, 74, pp. 51-56
  • Winston, G.W., Di Giulio, R.T., Prooxidant and antioxidant mechanisms in aquatic organisms (1991) Aquatic Toxicology, 19, pp. 137-161
  • Young, I., Woodside, J., Antioxidants in health and disease (2001) Journal of Clinical Pathology, 54, pp. 176-186
  • Zhou, J., Zhu, X., Cai, Z., Tributyltin toxicity in abalone (Haliotis diversicolor supertexta) assessed by antioxidant enzyme activity, metabolic response, and histopathology (2010) Journal of Hazardous Materials, 183, pp. 428-433

Citas:

---------- APA ----------
Primost, M.A., Sabatini, S.E., Di Salvatore, P., Ríos De Molina, M.C. & Bigatti, G. (2017) . Oxidative stress indicators in populations of the gastropod Buccinanops globulosus affected by imposex. Journal of the Marine Biological Association of the United Kingdom, 97(1), 35-42.
http://dx.doi.org/10.1017/S0025315415002155
---------- CHICAGO ----------
Primost, M.A., Sabatini, S.E., Di Salvatore, P., Ríos De Molina, M.C., Bigatti, G. "Oxidative stress indicators in populations of the gastropod Buccinanops globulosus affected by imposex" . Journal of the Marine Biological Association of the United Kingdom 97, no. 1 (2017) : 35-42.
http://dx.doi.org/10.1017/S0025315415002155
---------- MLA ----------
Primost, M.A., Sabatini, S.E., Di Salvatore, P., Ríos De Molina, M.C., Bigatti, G. "Oxidative stress indicators in populations of the gastropod Buccinanops globulosus affected by imposex" . Journal of the Marine Biological Association of the United Kingdom, vol. 97, no. 1, 2017, pp. 35-42.
http://dx.doi.org/10.1017/S0025315415002155
---------- VANCOUVER ----------
Primost, M.A., Sabatini, S.E., Di Salvatore, P., Ríos De Molina, M.C., Bigatti, G. Oxidative stress indicators in populations of the gastropod Buccinanops globulosus affected by imposex. J. Mar. Biol. Assoc. U.K. 2017;97(1):35-42.
http://dx.doi.org/10.1017/S0025315415002155