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The Gooseneck Barnacle (Pollicipes pollicipes) as a Candidate Sentinel Species for Coastal Contamination

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Abstract

The assessment of toxic effects caused by complex mixtures of contaminants in the marine environment requires previous validation of toxicological criteria, which may include biomarker end points with distinct biological meanings. This is the case of oxidative stress/phase II detoxification (glutathione-S-transferases activity), oxidative damage (thiobarbituric acid reactive substances), and neurotransmission (cholinesterase activity), which are likely to be affected after toxic insults by common marine pollutants. The main purpose of the present study was to assess potential biological alterations in the mollusk species Pollicipes pollicipes (gooseneck barnacle) caused by human contamination and seasonality, during a period of 1 year, in three different areas of the North Atlantic shore of Portugal. Our results indicate that fluctuations of the mentioned biomarkers were strongly related to seasonality, but they may also suffer influence by the already documented patterns of chemical contamination. Organisms collected in contaminated sampling sites (urban areas and oil refinery) showed greater levels of metabolic enzymes and increased levels of lipid peroxidation. These alterations were more evident during the summer, and, in some cases, spring months, suggesting an association between the presence of chemical stressors and temperature-dependent seasonal physiological fluctuations, which contribute to the modulation of the toxic response. In general terms, P. pollicipes was shown to be a promising organism in coastal biomonitoring programs, with an adequate sensitivity toward contamination and/or seasonal fluctuations. However, it is of the utmost importance to consider seasonal fluctuations in physiological parameters that modulate the toxic response. These factors can ultimately compromise the development and interpretation of data from marine biomonitoring programs if a thorough characterization of biological responses is not previously performed.

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References

  • Ahmad TA, Chaplin AE (1979) Seasonal variation in the anaerobic metabolism of the mussel Mytilus edulis (L.). Comp Biochem Physiol B 64:351–356

    Article  Google Scholar 

  • Barnes M (1996) Pedunculate cirripedes of the genus Pollicipes. Oceanogr Mar Biol 34:303–394

    Google Scholar 

  • Barreira LA, Mudge SM, Bebianno MJ (2007) Oxidative stress in the clam Ruditapes decussatus (Linnaeus 1758) in relation to polycyclic aromatic hydrocarbon body burden. Environ Toxicol 22:203–221

    Article  CAS  Google Scholar 

  • Beckett GJ, Hayes JD (1993) Glutathione S-transferases: biomedical applications. Adv Clin Chem 30:281–380

    Article  CAS  Google Scholar 

  • Ben-Khedher S, Jebali J, Kamel N, Banni M, Rameh M, Jrad A et al (2013) Biochemical effects in crabs (Carcinus maenas) and contamination levels in the Bizerta Lagoon: an integrated approach in biomonitoring of marine complex pollution. Environ Sci Pollut 20(4):2616–2631

    Article  CAS  Google Scholar 

  • Bonacci S, Ilaria C, Silvano F (2009) Cholinesterases in the Antarctic scallop Adamussium colbecki: characterization and sensitivity to pollutants. Ecotoxicol Environ Safe 72:1481–1488

    Article  CAS  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310

    Article  CAS  Google Scholar 

  • Cairrão E, Couderchet M, Soares AMVM, Guilhermino L (2004) Glutathione-S-transferase activity of Fucus spp. as a biomarker of environmental contamination. Aqua Toxicol 70(4):277–286

    Article  Google Scholar 

  • Chan B, Garm A, Høeg J (2008) Setal morphology and cirral setation of thoracican barnacle cirri: Adaptations and implications for thoracican evolution. J Zool 275:294–306

    Article  Google Scholar 

  • Correia A, Costa M, Luis O, Livingstone D (2003) Age-related changes in antioxidant enzyme activities, fatty acid composition and lipidperoxidation in whole body Gammarus locusta (Crustacea: Amphipoda). J Exp Mar Biol Ecol 289:83–101

    Article  CAS  Google Scholar 

  • Cuppen JG, Crum SJH, Heuvel HHVD, Smidt RA, Brink PJVD (2002) Effects of a mixture of two insecticides in freshwater microcosms: I. Fate of chlorpyrifos and lindane and responses of macroinvertebrates. Ecotoxicology 11:165–180

    Article  CAS  Google Scholar 

  • Ellman G, Courtney K, Andres V, Featherstone R (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    Article  CAS  Google Scholar 

  • Ferreira M, Moradas-Ferreira P, Reis-Henriques MA (2005) Oxidative stress biomarkers in two resident species, mullet (Mugil cephalus) and flounder (Platichthys flesus), from a polluted site in River Douro Estuary, Portugal. Aquat Toxicol 71(1):39–48

    Article  CAS  Google Scholar 

  • Filho DW, Tribess T, Gáspari C, Claudio FD, Torres MA, Magalhães ARM (2001) Seasonal changes in antioxidant defenses of the digestive gland of the brown mussel (Perna perna). Aquaculture 203(1–2):149–158

    Article  Google Scholar 

  • Fitzpatrick PJ, O’Halloran J, Sheehan D, Walsh AR (1997) Assessment of a glutathione S-transferase and related proteins in the gill and digestive gland of Mytilus edulis (L.), as potential organic pollution biomarkers. Biomarkers 2:51–56

    Article  CAS  Google Scholar 

  • Fossi M, Savelli C, Casini S (1998) Mixed function oxidase induction in Carcinus aestuarii. Field and experimental studies for the evaluation of toxicological risk due to Mediterranean contaminants. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 121:321–331

    Article  CAS  Google Scholar 

  • Frasco M, Fournier D, Carvalho F, Guilhermino L (2006) Cholinesterase from the common prawn (Palaemon serratus) eyes: catalytic properties and sensitivity to organophosphate and carbamate compounds. Aquat Toxicol 77:412–421

    Article  CAS  Google Scholar 

  • Frasco FM, Erzen I, Stojan J, Guilhermino L (2010) Localization and properties of cholinesterases in the common prawn (Palaemon serratus): a kinetic-histochemical study. Biol Bull 218:1–5

    CAS  Google Scholar 

  • French PW (1998) The impact of coal production on the sediment record of the Severn Estuary. Environ Pollut 103:37–43

    Article  CAS  Google Scholar 

  • Gabbott PA (1983) Developmental and seasonal metabolic activity in marine molluscs. In: Hochachka PW (ed) The mollusca: their ecology and physiology, vol 2. Academic Press, London, pp 165–217

    Google Scholar 

  • Garcia L, Castro B, Ribeiro R, Guilhermino L (2000) Characterization of cholinesterase from guppy (Poecilia reticulata) muscle and its in vitro inhibition by environmental contaminants. Biomarkers 5:274–284

    Article  CAS  Google Scholar 

  • Garcia-de la Parra M, Bautista-Covarrubias J, Rivera-de la Rosa N, Betancourt-Lozano M, Guilhermino L (2006) Effects of methamidophos on acetylcholinesterase activity, behavior, and feeding rate of the white shrimp (Litopenaeus vannamei). Ecotoxicol Environ Saf 65:372–380

    Article  CAS  Google Scholar 

  • Gowland B, Moffat C, Stagg R, Houlihan D, Davies I (2002) Cypermethrin induces glutathione S-transferase activity in the shore crab, Carcinus maenas. Mar Environ Res 54:169–177

    Article  CAS  Google Scholar 

  • Guilhermino L, Lacerda M, Nogueira A, Soares AMVM (2000) In vitro and in vivo inhibition of Daphnia magna acetylcholinesterase by surfactant agents: possible implications for contamination biomonitoring. Sci Total Environ 247:137–141

    Article  CAS  Google Scholar 

  • Habig W, Pabst M, Jakoby W (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  Google Scholar 

  • Hogan JW (1970) Water temperature as a source of variation in the specific activity of brain cholinesterase of bluegills. Bull Environ Contam Toxicol 5:347–354

    Article  CAS  Google Scholar 

  • Instituto Hidrográfico (2010/2011) Médias mensais da temperatura da água na estação de Leixões. Marinha, Portugal

  • Instituto Nacional de Estatística, I.P.—Portugal. Censos 2001, recenceamento total da população

  • Jbilo O, Toutant J, Vatsis K, Chatonnet A, Lockridge O (1994) Promoter and transcription start site of human and rabbit butyrylcholinesterase genes. J Biol Chem 269:20829–20837

    CAS  Google Scholar 

  • Jung J, Addison R, Shim R (2007) Characterization of cholinesterases in marbled sole Limanda yokohamae, and their inhibition in vitro by the fungicide iprobenfos. Mar Environ Res 63:471–478

    Article  CAS  Google Scholar 

  • Kaaya A, Najimi S, Ribera D, Narbonne J, Moukrim A (1999) Characterization of glutathione-S-transferases (GST) activities in Perna perna and Mytilus galloprovincialis used as a biomarker of pollution in the Agadir Marine Bay (south of Morocco). Bull Environ Contam Toxicol 62:623–629

    Article  CAS  Google Scholar 

  • Key P, Fulton M (2002) Characterization of cholinesterase activity in tissues of the grass shrimp (Palaemonetes pugio). Pesticide Biochem Physiol 72:186–192

    Article  CAS  Google Scholar 

  • Kopecka-Pilarczyk J (2013) Comparison of selected biomarkers in flounder (Platichthys flesus L.) from the Douro (Portugal) and Vistula (Poland) River estuaries. Mar Pollut Bull 73:70–77

    Article  CAS  Google Scholar 

  • Kuzmick D, Mitchelmore C, Hopkins W, Rowe C (2007) Effects of coal combustion residues on survival, antioxidant potential, and genotoxicity resulting from full-lifecycle exposure of grass shrimp (Palaemonetes pugio holthius). Sci Total Environ 373:420–430

    Article  CAS  Google Scholar 

  • Leiniö S, Lehtonen KK (2005) Seasonal variability in biomarkers in the bivalves Mytilus edulis and Macoma balthica from the northern Baltic Sea. Comp Biochem Physiol C Toxicol Pharmacol 140:408–421

    Article  Google Scholar 

  • Lima I, Moreira SM, Von Osten JR, Soares AMVM, Guilhermino L (2007) Biochemical responses of the marine mussel Mytilus galloprovincialis to petrochemical environmental contamination along the North-western coast of Portugal. Chemosphere 66(7):1230–1242

    Article  CAS  Google Scholar 

  • Livingstone DR (1993) Biotechnology and pollution monitoring: use of molecular biomarkers in the aquatic environment. J Chem Tech Biotechnol 57:195–211

    Article  CAS  Google Scholar 

  • Livingstone DR (2001) Contaminant-stimulated reactive oxygen production and oxidative damage in aquatic organisms. Mar Pollut Bull 42(8):656–666

    Article  CAS  Google Scholar 

  • Livingstone DR, Lemaire P, Matthews A, Peters LD, Porte C, Fitzpatrick PJ et al (1995) Assessment of the impact of organic pollutants on goby (Zosterisessor ophiocephalus) and mussel (Mytilus galloprovincialis) from the Venice Lagoon, Italy: Biochemical studies. Mar Environ Res 39(1–4):235–240

    Article  CAS  Google Scholar 

  • Madureira TV, Barreiro JC, Rocha MJ, Rocha E, Cass QB, Tiritan ME (2010) Spatiotemporal distribution of pharmaceuticals in the Douro River estuary (Portugal). Sci Total Environ 408(22):5513–5520

    Article  CAS  Google Scholar 

  • Molares J, Freire J (2003) Development and perspectives for community based management of the goose barnacle (Pollicipes pollicipes) fisheries in Galicia (NW Spain). Fish Res 65:485–492

    Article  Google Scholar 

  • Mora P, Michel X, Narbonne JF (1999) Cholinesterase activity as potential biomarker in two bivalves. Environ Toxicol Pharmacol 7:253–260

    Article  CAS  Google Scholar 

  • Moreira S, Guilhermino L (2005) The use of Mytilus galloprovincialis acetylcholinesterase and glutathione S-transferases activities as biomarkers of environmental contamination along the Northwest Portuguese coast. Environ Monit Assess 105:309–325

    Article  CAS  Google Scholar 

  • Mucha AP, Vasconcelos MT, Bordalo AA (2003) Macrobenthic community in the Douro estuary: relations with trace metals and natural sediment characteristics. Environ Pollut 121(2):169–180

    Article  CAS  Google Scholar 

  • Mucha AP, Vasconcelos MT, Bordalo AA (2005) Spatial and seasonal variations of the macrobenthic community and metal contamination in the Douro estuary (Portugal). Mar Environ Res 60(5):531–550

    Article  CAS  Google Scholar 

  • Nava JM, Lee DY, Ospina JH, Cai S-Y, Gaskins HR (2009) Genomic analyses reveal a conserved glutathione homeostasis pathway in the invertebrate chordate Ciona intestinalis. Physiol Genomics 39(3):183–194

    Article  CAS  Google Scholar 

  • Nunes B (2011) The use of cholinesterases in ecotoxicology. Rev Environ Contam Toxicol 212:29–59

    CAS  Google Scholar 

  • Nunes B, Carvalho F, Guilhermino L (2005) Characterization and use of the total head soluble cholinesterases from mosquitofish (Gambusia holbrooki) for screening of anticholinesterase activity. J Enzyme Inhib Med Chem 20(4):369–376

    Article  CAS  Google Scholar 

  • Oakes KD, Van Der Kraak GJ (2003) Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations exposed to pulp mill effluent. Aquat Toxicol 63:447–463

    Article  CAS  Google Scholar 

  • Payne J, Mathieu A, Melvin W, Fancey L (1996) Acetylcholinesterase, an old biomarker with a new future? Field trials in association with two urban rivers and a paper mill in Newfoundland. Mar Pollut Bull 23:225–231

    Article  Google Scholar 

  • Quintaneiro C, Monteiro M, Pastorinho R, Soares AMVM, Nogueira AJA, Morgado F et al (2006) Environmental pollution and natural populations: a biomarkers case study from the Iberian Atlantic coast. Mar Pollut Bull 52(11):1406–1413

    Article  CAS  Google Scholar 

  • Regoli F, Nigro M, Bertoli E, Principato G, Orlando E (1997) Defenses against oxidative stress in the Antarctic scallop Adamussium colbecki and effects of acute exposure to metals. Hydrobiologia 355:139–144

    Article  CAS  Google Scholar 

  • Ribeiro C, Tiritan ME, Rocha E, Rocha MJ (2009) Seasonal and spatial distribution of several endocrine-disrupting compounds in the Douro River Estuary, Portugal. Arch Environ Contam Toxicol 56(1):1–11

    Article  CAS  Google Scholar 

  • Robillard S, Beauchamp G, Laulier M (2003) The role of abiotic factors and pesticide levels on enzymatic activity in the freshwater mussel Anodonta cygnea at three different exposure sites. Comp Biochem Physiol C Toxicol Pharmacol 135:49–59

    Article  Google Scholar 

  • Rodrigues S, Caldeira C, Castro B, Gonçalves F, Nunes B, Antunes S (2011) Cholinesterase (ChE) inhibition in pumpkinseed (Lepomis gibbosus) as environmental biomarker: ChE characterization and potential neurotoxic effects of xenobiotics. Pestic Biochem Physiol 99(2):181–188

    Article  CAS  Google Scholar 

  • Swaileh KM (1996) Seasonal variations in the concentrations of Cu, Cd, Pb and Zn in Arctica islandica L. (Mollusca: Bivalvia) from Kiel Bay, Western Baltic Sea. Mar Pollut Bull 32:631–635

    Article  CAS  Google Scholar 

  • Timbrell JA (1998) Biomarker in toxicology. Toxicology 129:1–12

    Article  CAS  Google Scholar 

  • Tim-Tim A, Morgado F, Moreira S, Rangel R, Nogueira AJA, Soares A et al (2009) Cholinesterase and glutathione S-transferase activities of three mollusc species from the NW Portuguese coast in relation to the ‘Prestige’ oil spill. Chemosphere 77:1465–1475

    Article  CAS  Google Scholar 

  • Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: A review. Environ Toxicol Pharmacol 13:57–149

    Article  Google Scholar 

  • Vargas M, Geish M, Maciel FE, Cruz B, Filgueira D, Ferreira G et al (2010) Influence of the dark/light rhythm on the effects of UV radiation in then eyestalk of the crab Neohelice granulata. Comp Biochem Physiol 151:343–350

    Google Scholar 

  • Varó I, Navarro J, Amat F, Guilhermino L (2003) Effect of dichlorvos on cholinesterase activity of the European sea bass (Dicentrarchus labrax). Pestic Biochem Physiol 75:61–72

    Article  Google Scholar 

  • Vidal ML, Bassères A, Narbonne JF (2002) Seasonal variations of pollution biomarkers in two populations of Corbicula fluminea (Müller). Comp Biochem Physiol C Toxicol Pharmacol 131:133–151

    Article  Google Scholar 

  • Viñas L, Franco MA, Soriano JA, González JJ, Ortiz L, Bayona JM et al (2009) Accumulation trends of petroleum hydrocarbons in commercial shellfish from the Galician coast (NW Spain) affected by the Prestige oil spill. Chemosphere 75:534–541

    Google Scholar 

  • Wake H (2005) Oil refineries: a review of their ecological impacts on the aquatic environment. Estuar Coast Shelf Sci 62:131–140

    Article  CAS  Google Scholar 

  • Xuereb B, Noury P, Felten V, Garric J, Geffard O (2007) Cholinesterase activity in Gammarus pulex (Crustacea Amphipoda): characterization and effects of chlorpyrifos. Toxicology 236:178–189

    Article  CAS  Google Scholar 

  • Zeeshan M, Prasad S (2009) Differential response of growth, photosynthesis, antioxidant enzymes and lipid peroxidation to UV-B radiation in three cyanobacteria. S Afr J Bot 75:466–474

    Article  CAS  Google Scholar 

  • Zhang L, Qiu L, Wu H, Liu X, You L, Pei D et al (2012) Expression profiles of seven glutathione S-transferase (GST) genes from Venerupis philippinarum exposed to heavy metals and benzo[a]pyrene. Comp Biochem Physiol C Toxicol Pharmacol 155(3):517–552

    Article  CAS  Google Scholar 

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Acknowledgments

Portuguese Foundation for Science and Technology (FCT, Portugal) supported the Project BiOtoMetal (PTDC/AMB/70431/2006).

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Authors and Affiliations

  1. Departamento de Biologia, Faculdade de Ciências da Universidade do Porto, Rua do Campo Alegre s/n, Edifício FC4, 4169-007, Porto, Portugal

    A. S. Ramos & S. C. Antunes

  2. CESAM-Centro de Estudos do Ambiente e do Mar, Campus Universitário de Santiago, Universidade de Aveiro, 3810-193, Aveiro, Portugal

    F. Gonçalves & B. Nunes

  3. Departamento de Biologia, Campus Universitário de Santiago, Universidade de Aveiro, 3810-193, Aveiro, Portugal

    F. Gonçalves & B. Nunes

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  1. A. S. Ramos
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  2. S. C. Antunes
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  3. F. Gonçalves
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  4. B. Nunes
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Correspondence to S. C. Antunes.

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Ramos, A.S., Antunes, S.C., Gonçalves, F. et al. The Gooseneck Barnacle (Pollicipes pollicipes) as a Candidate Sentinel Species for Coastal Contamination. Arch Environ Contam Toxicol 66, 317–326 (2014). https://doi.org/10.1007/s00244-013-9978-1

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