Metals and As content in sediments and Manila clam Ruditapes philippinarum in the Tagus estuary (Portugal): Impacts and risk for human consumption
Introduction
Among coastal ecosystems, estuaries are considered highly productive areas, although deeply impacted by anthropogenic pressure (Covelli et al., 2012). They represent complex and dynamic aquatic environments, frequently exploited for fisheries, aquaculture, industries, transport and recreational activities (Lei et al., 2016). Estuaries worldwide are also impacted by discharges from urban sites, since pollutants are transported by the rivers and then into the sea through estuaries (Mitchell et al., 1999). As a consequence, these environments are constantly exposed to a wide variety of pollutants, as metals and metalloids (Hoffman et al., 2002), organic (Cardoso et al., 2016) and new emerging contaminants, such as pharmaceuticals (Heberer, 2002) and micro plastics (Zhao et al., 2015).
Metals and metalloids have demonstrated to be hazardous pollutants, due to their persistency, toxicity and bioaccumulative characteristics (Du Laing, 2011, Velez et al., 2015a). Considering that sediments of coastal ecosystems can act as a sink for metals and metalloids, the benthic fauna, closely in contact with the sediments, is particularly vulnerable to their contamination (Elliott and Quintino, 2007). Metals and metalloids are readily bioaccumulated by benthic fauna, including bivalves (Freitas et al., 2012, Velez et al., 2015a, de Oliveira et al., 2016, Gao et al., 2016, Vazquez-Luis et al., 2016) and polychaetes (Dean, 2008, Freitas et al., 2012), inducing toxic effects.
Metals and metalloids are considered typical environmental pollutants with prooxidant effects, due to their potential to induce the intracellular formation of reactive oxygen species (ROS) (Regoli and Giuliani, 2014). In fact, biochemical markers, including oxidative stress markers, became popular tools for detecting early toxic effects in aquatic organisms caused by these inorganic elements (e.g. Monserrat et al., 2007, Matozzo et al., 2012, Moschino et al., 2012, Velez et al., 2015b). The comparison between biochemical performance obtained from the same species in different environments will allow to assess the toxic impacts induced by different pollution types and/or levels and the effectiveness of the biological responses to specific environmental conditions (Chandurvelan et al., 2015, Velez et al., 2016a).
Bivalves have been recognized as appropriate bioindicator and/or sentinel species of environmental quality in aquatic systems (Cajaraville et al., 2000), not only due to their filter feeding behavior and benthic ecology (for a complete list of references, see Velez et al., 2016a) but also due to their commercial importance as seafood. Among bivalve species, the Manila (Asari) clam Ruditapes philippinarum (Adams & Reeve, 1850) is gaining increasing attention due to its wide geographic distribution and its ecological and economic relevance (Moschino et al., 2012). As a bivalve, the Manila clam presents high ability to accumulate elements in its tissues, with known capacities as bioindicator of elements pollution in estuarine environments (Sfriso et al., 2008, Matozzo et al., 2012, Moschino et al., 2012, Yang et al., 2013, Velez et al., 2015a, Velez et al., 2015b). Its worldwide distribution is strictly connected to its economic relevance for fisheries and aquaculture: originally distributed in the Indo-Pacific region, specifically in Japan, Korea and China (Gosling, 2003), Manila clam was introduced into the west coast of North America, Atlantic (Portugal, France, Spain, Ireland, England) and Mediterranean European coasts (France, Italy) (Gosling, 2003). As for Portugal, the Manila clam was firstly detected in 1984 in Ria Formosa (Algarve) (Ruano and Sobral, 2000) and, since then, established populations have been reported in estuarine systems all over the country including in the Óbidos lagoon (Velez et al., 2015b), Albufeira lagoon (Gaspar, 2010), Ria de Aveiro (e.g. Figueira et al., 2012), the Sado estuary (Gaspar, 2010), and the Tagus estuary (Gaspar, 2010, Chainho et al., 2015). Today this species represents one of the most important commercial bivalve, with the highest economic value among aquaculture shellfish products (FAO, 2013). A special concern regarding the occurrence of Manila clam in the Tagus estuary is its wider distribution and increasing abundance in recent years (Ramajal et al., 2016).
The occurrence of intensive Manila clam fishing - especially with mechanical dredges - can have negative effects on environments, particularly concerning impacts on benthic communities, sediment resuspension and increase of water turbidity (Pranovi et al., 2003, Pranovi et al., 2004). These effects have been already observed in Venice Lagoon, where intense Manila clam collection has been carried out for > 20 years, with dramatic effects on the lagoon environment, followed by a collapse of the clam production (see Boscolo Brusà et al., 2013 for a complete list of reference). Manila clam fishing in the Tagus Estuary is lacking a specific regulation, and many of illegal harvesters are actually involved in its collection and commerce (Ramajal et al., 2016). Moreover, the occurrence of illegal fishing can determinate a serious risk for human consumption, due to clam collection in microbiology or chemically polluted areas. It is well known that elements contamination in edible bivalves can determinate bioaccumulation in the trophic chain, especially in human consumers (Figueira et al., 2011) with consequent poisoning effects (Santos et al., 2014).
Taking into account the intense harvesting and commercial exploitation of Manila clam currently ongoing in the Tagus estuary, and the scarce informations regarding the environmental characterization of the exploited areas in terms of metals and As pollution, there is an urgent need to investigate the contamination levels in clams at the harvesting areas, and to reveal their use as bioindicator species and role as source of pollutants along the ecosystems trophic chain.
In this way, the aims of the present work were 1) to evaluate sediments contamination in the Tagus estuary, namely in terms of metals and As, within the areas used for Manila clam harvesting; 2) to quantify the metals and As content in the Manila clam, and the human health risks associated with its consumption; 3) to assess the physiological and biochemical performance of the species to different elements and concentration levels, and its possible role as a bioindicator of pollution in the Tagus estuary.
Section snippets
Study area
The Tagus estuary is one of the largest estuaries in Europe, covering an area of 320 km2: 40% of the estuary is composed of intertidal mudflats, and its eastern and southern areas contain extensive areas of salt marshes (Caçador et al., 1996). The main source of freshwater onto the Tagus estuary is the Tagus river, draining water from a total area of 86,629 km2, and representing the second most important hydrological basin in the Iberian Peninsula (Duarte and Caçador, 2012) in terms of
Physico-chemical characteristics of the investigated areas
Water salinity ranged from 24 (area A) to 40 (area F); sediment pH varied slightly among the study areas, ranging between 7.16 (area E) and 7.64 (area D) and sediment temperature ranged from 17.6 °C (area D) to 22.6 °C (area B). Sediment Eh ranged from − 23 mV (area E) to − 44 mV (area D) (see Table 1 for details).
The sediment grain size analysis showed that the areas with higher percentage of fine sediments - B and E - also presented higher organic matter content. In terms of fines content, these
Discussion
To our knowledge, this is the very first study investigating the metals and As concentrations in the Manila clam population from the Tagus estuary, relating the physiological and biochemical responses to the environmental contamination and clams bioaccumulation levels.
The results obtained for sediment contamination showed that, among the six investigated areas, B and E, respectively outer and inner Barreiro Bay, are the most contaminated in terms of metals and As. The lowest contamination
Conclusions
The present work provides novel data on the metals and As content from sediments and Manila clam samples of the Tagus estuary. Among the six investigated areas, significant differences were observed both for sediments and clams contamination: the most contaminated sediments were identified in areas B (outer) and E (inner) of the Barreiro Bay. The latter area E and area F (inner of Montijo Bay) showed the highest metals and As content in clams. Moreover, As concentrations in clams in all the
Acknowledgements
Authors would like to thank J. Ramajal (MARE, Faculty of Sciences, Lisbon University) and Cátia Velez (Department of Biology & CESAM, University of Aveiro) for their help with samples collection and field activities; Anthony P. Moreira for English editing and an anonymous referee for improving the paper.
Funding
This work has been supported by CESAM (UID/AMB/50017), FCT/MEC through national funds, and the co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020.
Stefania Chiesa and Rosa Freitas benefited from Post-Doctoral grants (SFRH/BPD/91923/2012 and SFRH/BPD/92258/2013), Ângela Almeida benefited from a Doctoral grant (SFRH/BD/110218/2015), all given by the National Funds through the Portuguese Science Foundation (FCT), supported by European Social Fund, “Programa
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