Laitano, M.V.; Díaz-Jaramillo, M.; Rodriguez, Y.E.; Ducós, E.; Panarello, H.O.; Fernández-Gimenez, A.V. "Linking stable isotopes and biochemical responses in Balanus glandula under sewage influence" (2018) Marine Pollution Bulletin. 127:505-511
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In the present study, we analyzed the influence of untreated sewage exposure on carbon (δ13C) and nitrogen (δ15N) isotopic composition and several biochemical responses in the barnacle Balanus glandula. The main objective was to evaluate whether changes in stable isotopes signature do reflect biochemical sub-lethal effects in a sewage influence gradient. Stable isotopes analysis showed differences in isotope signatures between close sewage influence and distant sites, being δ13C signatures stronger than that of δ15N. Regarding biochemical effects, although organisms close to the effluent would be clearly exposed to contaminants (increased GST activity) the oxidative stress would not be too evident (peroxidases and ACAP not affected). The most affected physiological aspect was the digestive one, reflected in increased alkaline proteases and lipases activities. A clear relation between δ15N and GST activity was found, showing to δ15N as an indicator of potential exposure to chemical contaminants. © 2017 Elsevier Ltd


Documento: Artículo
Título:Linking stable isotopes and biochemical responses in Balanus glandula under sewage influence
Autor:Laitano, M.V.; Díaz-Jaramillo, M.; Rodriguez, Y.E.; Ducós, E.; Panarello, H.O.; Fernández-Gimenez, A.V.
Filiación:Instituto de Investigaciones Marinas y Costeras (IIMyC), Universidad Nacional de Mar del Plata (UNMdP), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Laboratorio de Fisiología de Organismos Acuáticos y Biotecnología aplicada, Funes 3350, Mar del Plata, 7600, Argentina
IIMyC, UNMdP, CONICET, Laboratorio de Ecotoxicología y Contaminación Ambiental, Funes 3350, Mar del Plata, 7600, Argentina
INGEIS, Instituto de Geocronología y Geología Isotópica, CONICET-UBA, Universidad Nacional de Buenos Aires, Pabellón INGEIS - Ciudad Universitaria, Buenos Aires, 1428, Argentina
Palabras clave:Balanus; Biochemical alterations; Digestive enzymes; Sewage; Stable isotopes; Enzymes; Indicators (chemical); Isotopes; Sewage; Balanus; Biochemical alterations; Biochemical effects; Biochemical response; Chemical contaminants; Digestive enzymes; Isotopic composition; Stable isotopes; Alkalinity; alkaline proteinase; antioxidant capacity against peroxyl radical; carbon 13; glutathione transferase; monophenol monooxygenase; nitrogen 15; peroxidase; peroxy radical; triacylglycerol lipase; unclassified drug; alkaline proteinase; bacterial protein; biological marker; carbon; nitrogen; proteinase; sea water; triacylglycerol lipase; biochemistry; carbon isotope; crustacean; enzyme; isotopic composition; nitrogen isotope; sewage; stable isotope; sublethal effect; Article; Balanus glandula; chemical composition; controlled study; environmental exposure; environmental impact; enzyme activity; isotope analysis; molecular stability; nonhuman; oxidative stress; sewage; water contamination; water pollution indicator; analysis; animal; Argentina; barnacle; chemistry; drug effect; enzymology; metabolism; sewage; toxicity; water pollutant; Balanus; Balanus glandula; Thoracica; Animals; Argentina; Bacterial Proteins; Biomarkers; Carbon Isotopes; Endopeptidases; Environmental Exposure; Lipase; Nitrogen Isotopes; Seawater; Sewage; Thoracica; Water Pollutants, Chemical
Página de inicio:505
Página de fin:511
Título revista:Marine Pollution Bulletin
Título revista abreviado:Mar. Pollut. Bull.
CAS:carbon 13, 14762-74-4; glutathione transferase, 50812-37-8; monophenol monooxygenase, 9002-10-2; nitrogen 15, 14390-96-6; peroxidase, 9003-99-0; triacylglycerol lipase, 9001-62-1; carbon, 7440-44-0; nitrogen, 7727-37-9; proteinase, 9001-92-7; alkaline protease; Bacterial Proteins; Biomarkers; Carbon Isotopes; Endopeptidases; Lipase; Nitrogen Isotopes; Sewage; Water Pollutants, Chemical


  • Albentosa, M., Moyano, F.J., Differences in the digestive biochemistry between the intertidal clam, Ruditapes decussatus, and the subtidal clam, Venerupis pullastra (2009) Aquac. Int., 17, pp. 273-282
  • Amado, L.L., Garcia, M.L., Ramos, P.B., Freitas, R.F., Zafalon, B., Ferreira, J.L.R., Yunes, J.S., Monserrat, J.M., A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: application to evaluate microcystins toxicity (2009) Sci. Total Environ., 407, pp. 2115-2123
  • Barata, C., Lekumberri, I., Vila-Escalé, M., Prat, N., Porte, C., Trace metal concentration, antioxidant enzyme activities and susceptibility to oxidative stress in the tricoptera larvae Hydropsyche exocellata from the Llobregat river basin (NE Spain) (2005) Aquat. Toxicol., 74, pp. 3-19
  • Benedetti, M., Giuliani, M.E., Regoli, F., Oxidative metabolism of chemical pollutants in marine organisms: molecular and biochemical biomarkers in environmental toxicology (2015) Ann. N. Y. Acad. Sci., 1340, pp. 8-19
  • Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding (1976) Anal. Biochem., 72, pp. 248-254
  • Burnham, K.P., Anderson, D.R., Huyvaert, K.P., AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons (2011) Behav. Ecol. Sociobiol., 65, pp. 23-35
  • Carballeira, C., Espinosa, J., Carballeira, A., Linking δ15N and histopathological effects in molluscs exposed in situ to effluents from land-based marine fish farms (2011) Mar. Pollut. Bull., 62, pp. 2633-2641
  • Celis-Guerrero, L.E., García-Carreño, F.L., Navarrete Del Toro, M.A., Characterization of proteases in the digestive system of spiny lobster (Panulirus interruptus) (2004) Mar. Biotechnol., 6, pp. 262-269
  • Charron, L., Geffard, O., Chaumot, A., Coulaud, R., Jaffal, A., Gaillet, V., Dedourge-Geffard, O., Geffard, A., Consequences of lower food intake on the digestive enzymes activities, the energy reserves and the reproductive outcome in Gammarus fossarum (2015) PLoS One, 10, pp. 1-14
  • Chen, Z., Mayer, L.M., Weston, D.P., Bock, M.J., Jumars, P.A., Inhibition of digestive enzyme activities by copper in the guts of various marine benthic invertebrates (2002) Environ. Toxicol. Chem., 21, pp. 1243-1248
  • Coplen, T., Krouse, H., Böhlke, J., Reporting of nitrogen-isotope abundances (1992) Pure Appl. Chem., 64, pp. 907-908
  • Dedourge-Geffard, O., Charron, L., Hofbauer, C., Gaillet, V., Palais, F., Lacaze, E., Geffard, A., Geffard, O., Temporal patterns of digestive enzyme activities and feeding rate in gammarids (Gammarus fossarum) exposed to inland polluted waters (2013) Ecotoxicol. Environ. Saf., 97, pp. 139-146
  • Dolenec, T., Lojen, S., Dolenec, M., Lambaša, Ž., Dobnikar, M., Rogan, N., 15N and 13C enrichment in Balanus perforatus: tracers of municipal particulate waste in the murter sea (Central Adriatic, Croatia) (2006) Acta Chim. Slov., 53, pp. 469-476
  • Edwards, D.D.M., Distribution of Clostridium perfringens and fecal sterols in a benthic coastal marine environment (1998) Appl. Environ. Microbiol., 64, pp. 2596-2600
  • Fry, B., Stable Isotope Ecology, Stable Isotope Ecology (2006), Springer New York; Fytili, D., Zabaniotou, A., Utilization of sewage sludge in EU application of old and new methods - a review (2008) Renew. Sust. Energ. Rev., 12, pp. 116-140
  • Galloway, T.S., Depledge, M.H., Immunotoxicity in invertebrates: measurement and ecotoxicological relevance (2001) Ecotoxicology, 10, pp. 5-23
  • García-Carreño, F.L., The digestive proteases of langostilla (Pleuroncodes planipes, decapoda): their partial characterization, and the effect of feed on their composition (1992) Comp. Biochem. Physiol. B Comp. Biochem., 103, pp. 575-578
  • Gearing, P.J., Gearing, J.N., Maughan, J.T., Oviatt, C.A., Isotopic distribution of carbon from sewage-sludge and eutrophication in the sediments and food web of estuarine ecosystems (1991) Environ. Sci. Technol., 25, pp. 295-301
  • Gonfiantini, R., Standards for stable isotope measurements in natural compounds (1978) Nature, 271, pp. 534-536
  • Habig, W., Pabst, M., Jakoby, W., Glutathione S-transferase, the first enzymatic step in mercapturic acid formation (1974) J. Biol. Chem., 249, pp. 7130-7139
  • Iribarnegaray, M.A., Rodriguez-Alvarez, M.S., Moraña, L.B., Tejerina, W.A., Seghezzo, L., Management challenges for a more decentralized treatment and reuse of domestic wastewater in metropolitan areas (2017) J. Water Sanit. Hyg. Dev., ,, (In press)
  • Jemec, A., Drobne, D., Tišler, T., Sepčić, K., Biochemical biomarkers in environmental studies-lessons learnt from enzymes catalase, glutathione S-transferase and cholinesterase in two crustacean species (2010) Environ. Sci. Pollut. Res., 17, pp. 571-581
  • Kivaisi, A.K., The potential for constructed wetlands for wastewater treatment and reuse in developing countries: a review (2001) Ecol. Eng., 16, pp. 545-560
  • Laitano, M.V., Fernández-Gimenez, A.V., Are mussels always the best bioindicators? Comparative study on biochemical responses of three marine invertebrate species to chronic port pollution (2016) Bull. Environ. Contam. Toxicol., 97, pp. 50-55
  • Laitano, M.V., Silva Barni, M., Costa, P.G., Cledón, M., Fillmann, G., Miglioranza, K., Panarello, H., Different carbon sources affect PCB accumulation by marine bivalves (2016) Mar. Environ. Res., 113, pp. 62-69
  • Lamela, R.E.L., Silveira Coffigny, R., Cruz Quintana, Y., Martínez, M., Phenoloxidase and peroxidase activity in the shrimp Litopenaeus schmitti, Pérez-Farfante and Kensley (1997) exposed to low salinity (2005) Aquac. Res., 36, pp. 1293-1297
  • Lima, I., Moreira, S.M., Osten, J.R.-V., Soares, A.M.V.M., Guilhermino, L., Biochemical responses of the marine mussel Mytilus galloprovincialis to petrochemical environmental contamination along the North-western coast of Portugal (2007) Chemosphere, 66, pp. 1230-1242
  • López Gappa, J.J., Tablado, A., Magaldi, N.H., Influence of sewage pollution on a rocky intertidal community dominated by the mytilid Brachidontes rodriguezi (1990) Mar. Ecol. Prog. Ser., 63, pp. 163-175
  • Machado, A.A.D.S., Wood, C.M., Bianchini, A., Gillis, P.L., Responses of biomarkers in wild freshwater mussels chronically exposed to complex contaminant mixtures (2014) Ecotoxicology, 23, pp. 1345-1358
  • Mancinelli, G., Vizzini, S., Assessing anthropogenic pressures on coastal marine ecosystems using stable CNS isotopes: state of the art, knowledge gaps, and community-scale perspectives (2015) Estuar. Coast. Shelf Sci., 156, pp. 195-204
  • Morrissey, C.A., Boldt, A., Mapstone, A., Newton, J., Ormerod, S.J., Stable isotopes as indicators of wastewater effects on the macroinvertebrates of urban rivers (2013) Hydrobiologia, 700, pp. 231-244
  • Oakes, J.M., Eyre, B.D., Wastewater nitrogen and trace metal uptake by biota on a high-energy rocky shore detected using stable isotopes (2015) Mar. Pollut. Bull., 100, pp. 406-413
  • Palmer, C.V., Bythell, J.C., Willis, B.L., A comparative study of phenoloxidase activity in diseased and bleached colonies of the coral Acropora millepora (2011) Dev. Comp. Immunol., 35, pp. 1098-1101
  • Peterson, B.J., Fry, B., Stable isotopes in ecosystem studies (1987) Annu. Rev. Ecol. Syst., 18, pp. 293-320
  • Piola, R.F., Moore, S.K., Suthers, I.M., Carbon and nitrogen stable isotope analysis of three types of oyster tissue in an impacted estuary (2006) Estuar. Coast. Shelf Sci., 66, pp. 255-266
  • Post, D.M., Using stable isotopes to estimate trophic position: models, methods, and assumptions (2002) Ecology, 83, pp. 703-718
  • Raunkjᴂr, K., Hvited-Jacobsen, T., Nielsen, P., Measurement of pools of protein, carbohydrate and lipid in domestic wastewater (1994) Water Res., 28, pp. 251-262
  • Rogers, K.M., Stable carbon and nitrogen isotope signatures indicate recovery of marine biota from sewage pollution at Moa Point, New Zealand (2003) Mar. Pollut. Bull., 46, pp. 821-827
  • Sato, T., Qadir, M., Yamamoto, S., Endo, T., Zahoor, A., Global, regional, and country level need for data on wastewater generation, treatment, and use (2013) Agric. Water Manag., 130, pp. 1-13
  • Söderhäll, K., Cerenius, L., Role of the prophenoloxidase-activating system in invertebrate immunity (1998) Curr. Opin. Immunol., 10, pp. 23-28
  • Spivak, E.D., Schwindt, E., Balanomorfos (Cirripedia: Thoracica) (2014) Biodiversidad de Artrópodos Argentinos Vol. 3. Sociedad Entomológica Argentina, pp. 1-18. , S. Roig-Juñent L. Claps J. Morrone
  • Tablado, A., Gappa, J.L., Morphometric diversity of the pulmonate limpet Siphonaria lessoni in different coastal environments (2001) Sci. Mar., 65, pp. 33-41
  • Tablado, A., López Gappa, J.J., Magaldi, N.H., Growth of the pulmonate limpet Siphonaria lessoni (Blainville) in a rocky intertidal area affected by sewage pollution (1994) J. Exp. Mar. Biol. Ecol., 175, pp. 211-226
  • Toyoda, S., Suzuki, Y., Hattori, S., Yamada, K., Fujii, A., Yoshida, N., Kouno, R., Shiomi, H., Isotopomer analysis of production and consumption mechanisms of N2O and CH4 in an advanced wastewater treatment system (2011) Environ. Sci. Technol., 45, pp. 917-922
  • Versaw, W.K., Cuppett, S.L., Winters, D.D., Willams, L.E., An improved colorimetric assay for bacterial lipase in nonfat dry milk (1989) J. Food Sci., 54, pp. 1557-1558
  • Vizzini, S., Mazzola, A., The effects of anthropogenic organic matter inputs on stable carbon and nitrogen isotopes in organisms from different trophic levels in a southern Mediterranean coastal area (2006) Sci. Total Environ., 368, pp. 723-731
  • Waldron, S., Tatner, P., Jack, I., Arnott, C., The impact of sewage discharge in a marine embayment: a stable isotope reconnaissance (2001) Estuar. Coast. Shelf Sci., 52, pp. 111-115
  • Zanette, J., Monserrat, J.M., Bianchini, A., Biochemical biomarkers in barnacles Balanus improvisus: pollution and seasonal effects (2015) Mar. Environ. Res., 103, pp. 74-79


---------- APA ----------
Laitano, M.V., Díaz-Jaramillo, M., Rodriguez, Y.E., Ducós, E., Panarello, H.O. & Fernández-Gimenez, A.V. (2018) . Linking stable isotopes and biochemical responses in Balanus glandula under sewage influence. Marine Pollution Bulletin, 127, 505-511.
---------- CHICAGO ----------
Laitano, M.V., Díaz-Jaramillo, M., Rodriguez, Y.E., Ducós, E., Panarello, H.O., Fernández-Gimenez, A.V. "Linking stable isotopes and biochemical responses in Balanus glandula under sewage influence" . Marine Pollution Bulletin 127 (2018) : 505-511.
---------- MLA ----------
Laitano, M.V., Díaz-Jaramillo, M., Rodriguez, Y.E., Ducós, E., Panarello, H.O., Fernández-Gimenez, A.V. "Linking stable isotopes and biochemical responses in Balanus glandula under sewage influence" . Marine Pollution Bulletin, vol. 127, 2018, pp. 505-511.
---------- VANCOUVER ----------
Laitano, M.V., Díaz-Jaramillo, M., Rodriguez, Y.E., Ducós, E., Panarello, H.O., Fernández-Gimenez, A.V. Linking stable isotopes and biochemical responses in Balanus glandula under sewage influence. Mar. Pollut. Bull. 2018;127:505-511.