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  • Source and impact of lead contamination on δ-aminolevulinic acid dehydratase activity in several marine bivalve species along the Gulf of Cadiz
    Publication . Company, Rui; Serafim, M.A.; Lopes, Belisandra; Cravo, Alexandra; Kalman, J.; Riba, I.; DelValls, T. A.; Blasco, J.; Delgado, J.; Sarmiento, A . M.; Nieto, J. M.; Shepherd, T. J.; Nowell, G.; Bebianno, Maria João
    Coastal areas and estuaries are particularly sensitive to metal contamination from anthropogenic sources and in the last few decades the study of space-time distribution and variation of metals has been extensively researched. The Gulf of Cadiz is no exception, with several rivers draining one of the largest concentrations of sulphide deposits in the world, the Iberian Pyrite Belt (IPB). Of these rivers, the Guadiana, one of the most important in the Iberian Peninsula, together with smaller rivers like the Tinto and Odiel, delivers a very high metal load to the adjacent coastal areas. The purpose of this work was to study the source and impact of lead (Pb) drained from historical or active mining areas in the IPB on the activity of a Pb inhibited enzyme (δ-aminolevulinic acid dehydratase, ALAD) in several bivalve species along the Gulf of Cadiz. Seven marine species (Chamelea gallina, Mactra corallina, Donax trunculus, Cerastoderma edule, Mytilus galloprovincialis, Scrobicularia plana and Crassostrea angulata) were collected at 12 sites from Mazagón, near the mouth of the rivers Tinto and Odiel (Spain), to Cacela Velha (Ria Formosa lagoon system, Portugal). Lead concentrations, ALAD activity and lead isotope ratios ((206)Pb/(204)Pb, (207)Pb/(204)Pb and (208)Pb/(204)Pb) were determined in the whole soft tissues. The highest Pb concentrations were determined in S. plana (3.50±1.09 μg g(-1) Pb d.w.) and D. trunculus (1.95±0.10 μg g(-1) Pb d.w.), while M. galloprovincialis and C. angulata showed the lowest Pb levels (<0.38 μg g(-1) Pb d.w.). In general, ALAD activity is negatively correlated with total Pb concentration. However this relationship is species dependent (e.g. linear for C. gallina ALAD=-0.36[Pb]+0.79; r=0.837; or exponential for M. galloprovincialis ALAD=2.48e(-8.3[Pb]); r=0.911). This indicates that ALAD activity has considerable potential as a biomarker of Pb and moreover, in marine bivalve species with different feeding habits. Lead isotope data showed significant seasonal and spatial changes in bivalve isotopic composition reflecting seasonal and geographic differences in bioaccumulation. Within the study area, Pb can be modelled as a mixing between geogenic Pb and mine-related, discharges of Pb from the IPB. For some sites at the mouth of the Guadiana River, the bivalves show contamination from other anthropogenic sources, such as leaded boat/aviation fuel and/or leaded paint. Finally, the study demonstrates convincingly the need to consider species-specific variation when using bivalve ALAD activity as a biomarker for Pb.
  • Integrated approach to assess ecosystem health in harbor areas
    Publication . Bebianno, Maria João; Pereira, C.; Rey, F.; Cravo, Alexandra; Duarte, D. N.; D'Errico, G.; Regoli, F.
    Harbors are critical environments with strategic economic importance but with potential environmental impact: health assessment criteria are a key issue. An ecosystem health status approach was carried out in Portimão harbor as a case-study. Priority and specific chemical levels in sediments along with their bioavailability in mussels, bioassays and a wide array of biomarkers were integrated in a biomarker index (IBR index) and the overall data in a weight of evidence (WOE) model. Metals, PAHs, PCBs and HCB were not particularly high compared with sediment guidelines and standards for dredging. Bioavailability was evident for Cd, Cu and Zn. Biomarkers proved more sensitive namely changes of antioxidant responses, metallothioneins and vittellogenin-like proteins. IBR index indicated that site 4 was the most impacted area. Assessment of the health status by WOE approach highlighted the importance of integrating sediment chemistry, bioaccumulation, biomarkers and bioassays and revealed that despite some disturbance in the harbor area, there was also an impact of urban effluents from upstream.
  • Genotoxicity of copper oxide and silver nanoparticles in the mussel Mytilus galloprovincialis
    Publication . Gomes, Tânia; Araújo, Olinda; Pereira, Rita; Catarina Almeida, Ana; Cravo, Alexandra; Bebianno, Maria João
    Though there is some information on cytotoxicity of copper nanoparticles and silver nanoparticles on human cell lines, there is no information on their genotoxic and cytotoxic behaviour in bivalve molluscs. The aim of this study was to investigate the genotoxic impact of copper oxide and silver nanoparticles using mussels Mytilus galloprovincialis. Mussels were exposed to 10 μg L⁻¹ of CuO nanoparticles and Cu²⁺ and Ag nanoparticles and Ag⁺ for 15 days to assess genotoxic effects in hemocytes using the comet assay. The results obtained indicated that copper and silver forms (nanoparticles and ionic) induced DNA damage in hemolymph cells and a time-response effect was evident when compared to unexposed mussels. Ionic forms presented higher genotoxicity than nanoparticles, suggesting different mechanisms of action that may be mediated through oxidative stress. DNA strand breaks proved to be a useful biomarker of exposure to genotoxic effects of CuO and Ag nanoparticles in marine molluscs.
  • A multibiomarker approach in Mytilus galloprovincialis to assess environmental quality
    Publication . Cravo, Alexandra; Lopes, Belisandra; Serafim, M.A.; Company, Rui; Barreira, Luísa; Gomes, Tânia; Bebianno, Maria João
    A multibiomarker approach was carried out for the first time in the South Portuguese Coast using Mytilus galloprovincialis, to assess environmental quality, establish if there are adverse biological responses associated to different sources of anthropogenic contamination and to determine spatial and seasonal trends. For this purpose the battery of biomarkers selected was: superoxide dismutase (SOD), catalase (CAT), glutathione peroxidases (GPx total and Se dependent), Cytochrome P450 component system, Glutathione-S-transferase (GST) and acetylcholinesterase (AChE), metallothionein (MT) and lead-delta-aminolevulinic acid dehydratase (ALAD), lipid peroxidation (LPO) and Condition Index (CI) along with the determination of PAHs and metals (Cd, Cu, Ni, Pb and Zn). Results show that despite the levels of both organic and metallic contaminants in these eight spots in the South Coast of Portugal not being particularly high compared with other contaminated/polluted sites worldwide, the selected battery of biomarkers responded efficiently to the environmental changes and allowed an environmental assessment between seasons and sites. Different spatial and seasonal responses were evident along the South Coast of Portugal, meaning that the contamination is not homogeneous. This does not only reflect different competition, origin and intensity of contamination, but also different environmental conditions (e.g. temperature, salinity). Along the South Portuguese Coast site 8 was the most contaminated, while site 2 was considered the least contaminated. Despite environmental factors possibly causing difficulties in the general interpretation of biomarker data, those that better responded to environmental contamination were CYP450, SOD-mit and T-GPx for the summation SigmaPAHs, MT (digestive gland) for metals (especially Cu), ALAD for Pb and LPO for both organic and metallic contamination. These biomarkers were also positively correlated with temperature in summer, revealing this as a more stressful/critical season. In future environmental contamination assessments there is no need to analyse the components b5, P418, NADH and NADPH of phase I MFO system, and MT in the gills, since their responses are not evident.
  • Genotoxicity in two bivalve species from a coastal lagoon in the south of Portugal
    Publication . Catarina Almeida, Ana; G. Pereira, Catarina; Gomes, Tânia; Cardoso, Cátia; Bebianno, Maria João; Cravo, Alexandra
    DNA damage was evaluated by comet assay in the haemolymph of two bivalve species Ruditapes decussatus and Mytilus galloprovincialis from the Ria Formosa lagoon (south Coast of Portugal). Clams and mussels were sampled from sites close to each other to determine interspecific responses to similar environmental conditions, considering also seasonal and gender differences. Coupled with genotoxic effect, another damage biomarker (lipid peroxidation) was analysed to verify if the conditions that instigate DNA damage can be related with injury to cell membranes. For both species, DNA damage was low, reflecting the low levels of genotoxic contaminants in the lagoon, and no interspecific differences were found. However, seasonal differences were established for both bivalve species, reflecting higher environmental stress in summer. Regarding gender susceptibility, only clams showed differences in percentage of Tail DNA, with females more sensitive to DNA damage than males. Additionally, results for clams point out that factors responsible for LPO may not be the same as those causing genotoxicity. This study demonstrated that DNA damage is a sensitive biomarker to discriminate spatial, temporal and gender differences, being an appropriate biomarker for genotoxicity evaluation even in places of low contamination, such as the Ria Formosa lagoon.
  • Metal concentrations in the shell of Bathymodiolus azoricus from contrasting hydrothermal vent fields on the mid-Atlantic ridge
    Publication . Cravo, Alexandra; Foster, P.; Catarina Almeida, Ana; Bebianno, Maria João; Company, Rui
    Specimens of Bathymodiolus azoricus were sampled along the Mid-Atlantic Ridge at the Menez Gwen, Lucky Strike and Rainbow hydrothermal fields. Individual shells (n = 51), through the weight range 0.62 to 15.70 g, were analyzed for their magnesium, strontium, iron, manganese, copper, zinc and cadmium concentrations. Amongst the marine molluscs the shell of B. azoricus is confirmed as being particularly impoverished in strontium (mean 943 microg g(-1)). Trace metal concentrations in the shells decreased in the order Fe> Mn> Zn> Cu> Cd. Despite originating from trace metal rich environments mean concentrations were low (37.9, 13.2, 10.7, 1.1 and 0.7 microg g(-1), respectively). Irrespective of geographical origin magnesium, strontium and copper concentrations were primarily dictated by shell weight. In contrast cadmium concentrations were elevated in shells from the Rainbow field and ambient seawater chemistry imparted site specific chemical fingerprints to the shells with respect to the iron to manganese ratio.
  • DNA damage as a biomarker of genotoxic contamination in Mytilus galloprovincialis from the south coast of Portugal
    Publication . Catarina Almeida, Ana; G. Pereira, Catarina; Gomes, Tânia; Bebianno, Maria João; Cravo, Alexandra
    DNA damage was evaluated in the haemolymph of Mytilus galloprovincialis from nine sites along the south coast of Portugal using the comet assay. DNA damage was low, in the same range of sites considered to suffer low impact from genotoxic contaminants. Even so, differences between sites, seasons and genders were found. Highest values were in mussels from the main estuaries and the fishery harbour, reflecting higher genotoxin levels, whereas the lowest values can be used as a baseline for future work. Non-contaminant related factors (e.g. temperature and oxygen) were also shown to influence DNA damage. Between seasons, highest values were in summer related not only to the increase of tourism in this region (∼10-fold), but also to temperature. Between genders, males were found to be more sensitive. The condition index was also generally higher in summer. Lipid peroxidation, another damage biomarker, was measured in gills to assess if there is any association between the responses of both biomarkers and if they are similarly affected by the same environmental conditions. LPO like DNA damage was higher in summer. This work confirms that DNA damage is a sensitive biomarker to discriminate genotoxic contamination, even in areas considered to suffer low impact from genotoxins.
  • Metals in the shell of Bathymodiolus azoricus from a hydrothermal vent site on the Mid-Atlantic Ridge
    Publication . Cravo, Alexandra; Foster, P.; Catarina Almeida, Ana; Company, Rui; Cosson, R.P.; Bebianno, Maria João
    Specimens of the mussel Bathymodiolus azoricus were collected from Menez Gwen, a relatively shallow (850 m) hydrothermal vent field on the Mid-Atlantic Ridge. Each bivalve shell (n = 21) was individually cleaned by selective chemical. The residual crystal matrix of each shell was individually analysed for the concentrations of the minor elements magnesium and strontium and the trace elements iron, manganese, copper and zinc. The chemical composition of the crystal matrix is unusual. B. azoricus is identified as a species having one of the most strontium impoverished shells amongst the marine molluscs. For a bimineral species the magnesium concentration is also extraordinary low. Despite originating from a trace metal rich environment; the metal concentrations in the shells were exceptionally low. Mean concentrations of iron, manganese, copper and zinc were 20.6, 3.7, 0.6 and 9.4 microg g(-1) respectively. Minor and trace element concentrations exhibited a marked intra-population variability. Copper concentrations increased and iron and zinc concentrations decreased with increasing shell weight. Due to its insensitivity to the high environmental levels of trace elements and the variability in intra-population concentrations induced by shell weight the crystal matrix of the shell of B. azoricus has little potential for use in environmental trace metal monitoring in areas contiguous to deep-sea hydrothermal vents.
  • A multi-biomarker approach in cross-transplanted mussels Mytilus galloprovincialis
    Publication . Serafim, M.A.; Lopes, Belisandra; Company, Rui; Cravo, Alexandra; Gomes, Tânia; Serrão Sousa, Vânia; Bebianno, Maria João
    The present work integrates the active biomonitoring (ABM) concept in mussels Mytilus galloprovincialis from the South coast of Portugal transplanted during 28 days between two sites with different sources of contamination, and vice versa, in order to assess biological effects in these mussels. For that purpose a multibiomarker approach was used. The suit of biomarkers indicative of metal contamination were metallothioneins (MT) and the enzyme δ-aminolevulinic acid dehydratase (ALAD), for organic contamination mixed function oxidase system (MFO), glutathione-S-transferase (GST) and acetylcholinesterase (AChE), as oxidative stress biomarkers superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx) and lipid peroxidation (LPO). These biomarkers were used to determine an index to evaluate the stress levels in these two sites. Site A is strongly influenced by metallic contamination, with higher Cu, Cr and Pb in M. galloprovincialis, as well as higher MT levels, antioxidant enzymes activities and LPO concentrations, and lower ALAD activity. In site B organic compounds (PAHs) are prevalent and native mussels show higher activities of the MFO system components and GST. Transplanted mussels had significant alterations in some biomarkers that reflect the type of contaminants present in each site, which demonstrates the primary role of the environment in determining the physiological characteristics of resident mussels. Therefore the application of ABM using a battery of biomarkers turns out to be a useful approach in sites where usually complex mixtures of contaminants occurs. In this study the biomarkers that better differentiate the impact of different contaminants at each site were MT, CYP450, SOD and CAT.
  • Using biochemical and isotope geochemistry to understand the environmental and public health implications of lead pollution in the lower Guadiana River, Iberia: A freshwater bivalve study
    Publication . Company, Rui; Serafim, Angela; Lopes, Belisandra; Cravo, A.; Shepherd, T. J.; Pearson, G.; Bebianno, Maria João; Cravo, Alexandra
    Lead is a natural component of aquatic ecosystems with no known biological role and is highly toxic. Its toxicity stems from its ability to mimic biologically important metals and to produce membrane damage through lipid peroxidation (LPO). Most lead poisoning symptoms are thought to occur by interfering with an essential enzyme, delta-aminolevulinic acid dehydratase (ALAD), the activity of which is markedly inhibited by lead. The purpose of this work was to study the levels and effects of lead pollution (responses of ALAD and oxidative stress biomarker LPO) in the freshwater bivalve Corbicula fluminea along the lower Guadiana River (Portugal and Spain); a major river system impacted by historic mining pollution and more recent anthropogenic inputs. The results show that the enzymatic activity of ALAD is negatively correlated with the total Pb concentration of the whole tissue suggesting that ALAD has considerable potential as a biomarker of lead exposure in C. fluminea. To identify the sources of lead to which bivalves have been exposed, high precision (206)Pb/(204)Pb, (207)Pb/(204)Pb, (208)Pb/(204)/Pb ratios for C. fluminea confirm that historical mining activities in the Iberian Pyrite Belt are the dominant source of lead pollution in the lower Guadiana River. The isotope patterns however exhibit marked seasonal and geographic variation in response to rainfall and river water management. Locally, other anthropogenic sources of lead have been detected in C. fluminea close to population centres, thus adding to its versatility as a freshwater bio-indicator. Overall, the study highlights the value of natural ecosystems as monitors of water quality and their importance for public health assessment and surveillance.