Elsevier

Estuarine, Coastal and Shelf Science

Volume 209, 30 September 2018, Pages 136-148
Estuarine, Coastal and Shelf Science

Biogeochemical dynamics and bioaccumulation processes in Manila clam: Implications for biodiversity and ecosystem services in the Ria de Aveiro Lagoon

https://doi.org/10.1016/j.ecss.2018.04.029Get rights and content

Highlights

  • Metal(loid) fate has been investigated in the Ria de Aveiro Lagoon (Portugal).

  • Bioaccumulation patterns have been studied together with geochemical speciation data.

  • Multiple driving forces interacted together to determine site-specific impacts.

  • Bioaccumulation processes in Manila clam were observed for Cd, Zn and especially As.

  • The Ílhavo area should be considered the most dangerous in terms of clam consumption.

Abstract

The present work was carried out in the Ria de Aveiro Lagoon (Portugal) to better understand the dynamics driving the bioaccumulation processes in edible bivalves, namely in the Manila clam Ruditapes philippinarum. For the first time, a holistic approach was applied, collecting data on sediment physico-chemical characteristics and its contamination, geochemical speciation and metal(loid) bioaccumulation in clams, from three exploited areas of the lagoon (Costa Nova, Torreira, Ílhavo). The Ria de Aveiro Lagoon is part of the Natura 2000 network, has the designation of Special Protection Area (SPA), contains Sites of Community Importance (SCI), it is protected by the EU Birds Directive (79/109/CEE) and includes a natural reserve in its northern part. Specifically concerning the metal(loid) occurrence, the monitoring and the identification of contaminated sites in protected areas are priorities, to improve the biodiversity conservation efforts and to ensure the correct management of natural resources.

Results showed that multiple driving forces interacted together to determine site-specific impacts, resulting in different risks at local scale for the transferring of the metal(loid)s to the trophic chain. Hydrodynamics played a major role driving the occurrence of depositional or ablative sites, influencing the granulometric composition of sediments and their contamination; metal(loid) chemical forms were then determinated by multiple factors like pH, redox potential and organic matter content. The geochemical speciation data showed that the Ílhavo area should be considered the most dangerous in terms of clam consumption, since in case of environmental changes, possible conversion of the elements from the potentially bioavailable forms to the bioavailable ones can occur. Moreover, bioaccumulation processes in Manila clam were observed for Cd, Zn and especially As, the latter representing serious risk for consumer safety throughout clam consumption.

Introduction

Coastal lagoons are considered as highly unpredictable environments, subjected to spatial and temporal bio-geochemical variability (Ferrarin et al., 2010). Moreover, they are among the most productive ecosystems (Covelli et al., 2012), deeply exploited for human activities. Anthropogenic pressures like industries, agriculture, sewage discharges and aquaculture has often altered the fresh and saltwater inputs, nutrient loading, sedimentation and accumulation of contaminants (Covelli et al., 2012). Transitional environments like coastal lagoons are of primarily importance, due to their filter role between the landscape and the Sea, influencing the fate of contaminants in marine ecosystems (Du Laing, 2011). In fact, due to their key role coastal lagoons are also considered as a Priority Habitat for conservation in Europe.

The Ria de Aveiro Lagoon, located in the North-Western Portugal, represents an interesting example of a shallow-water ecosystem. It is formed by several branches and it is characterized by a network of saltmarshes and channels resulting in a very irregular and complex geometry (Martins et al., 2015a; b). The lagoon has been subjected to anthropogenic pressures (Martins et al., 2015a; b), particularly a mercury enriched effluent from a chloralkali industry which has contaminated a specific area of this ecosystem, the so called Laranjo Bay (Castro et al., 2009; Freitas et al., 2012a; b; Pereira et al., 2009). Moreover, as the lagoon has very complex hydrodynamics (Dias et al., 1999) affecting the biological, chemical and geological processes, recent mineralogical and geochemical data collected from this ecosystem showed the occurrence of both low and moderately polluted sites (Martins et al., 2015a; b; Velez et al., 2015a).

It must be underlined that, particularly in multi-use protected areas, like the Ria de Aveiro Lagoon, it is fundamental to identify the risks related to pollution and transferring of the contaminants among abiotic and biotic compounds, both for biodiversity conservation and human health.

Among contaminants, inorganic compounds such as metals and metalloids are considered particularly dangerous, due to their persistence, toxicity and bioaccumulative capabilities (Du Laing, 2011). Elements are transported by freshwaters as soluble phases or adsorbed on suspended particles (particularly bounded to fine particles and organic matter which are excellent metal(loid)-scavengers) (De Groot et al., 1976; Förstner and Wittmann, 1979; Luoma and Rainbow, 2008). Once they reach the interface between freshwater and saltwater occurring in transitional environments, they are subjected to chemical-physical transformations which may shift their aggregative properties while entering in a different hydric circulation pattern (Du Laing, 2011). Additionally, site-specific hydrological and hydrodynamic conditions may lead to the establishment of specific areas enriched of contaminants, posing risks for the transitional ecosystems. According to the granulometric characteristics, the particles reaching the transitional environments have a different fate: the largest particles keep their individual dimensions and their depositional behavior depends solely on hydrodynamic and gravitational factors (Aston and Chester, 1976). On the opposite, particles of smaller dimensions are influenced by a series of processes (such as coagulation and flocculation), which modify their dimensional distribution and depositional route (Aston and Chester, 1976).

Another important factor to be considered is the occurrence of organic matter which, along with oxides/hydroxides of Fe and Mn, can form flocs with fine-grained particles. Flocs sediment in a colloidal form together with the newly formed aggregates, also drag soluble metal(loid) chemical forms (Argese et al., 1992) and stabilize the majority of them in the sediments (Aston and Chester, 1976; Burton, 1976). Besides granulometry and organic matter, also hydrodynamics, biogeochemical processes and environmental conditions (microbial activities, redox potential, pH, dissolved O2, salinity and temperature) can determine both spatial distribution and bioavailability of elements in transitional environments (Gambrell et al., 1980).

Metal(loid)s are distributed among a variety of association forms, differing in the intensity of metal-matrix bonds: as a consequence, each of these forms exhibits a different potential for remobilization and a different bioavailability (Argese and Bettiol, 2001). It must be stated that metal(loid)s transferring from the soluble phase to the sediment, and from the sediment to the soluble phase, it is not a definitive process, instead it is always changing due to the variable environmental conditions; elements can be continuously solubilized passing from a chemical form to another (Gambrell et al., 1980).

As a consequence, total metal(loid) content data do not provide sufficient information about the real risk for bioaccumulation in biotic matrixes, posed by contaminated sediments. On the opposite, metal(loid) partitioning by geochemical speciation can help in evaluating the amount of directly and/or potentially bioavailable element fractions (Argese et al., 2003).

Edible bivalves are well-know bioindicators which can supply the direct estimation of bioavailability of toxic compounds as metal(loid)s (Argese et al., 2005; Bettiol et al., 2008). They have been widely investigated to determine the risks associated with their consumption (Sfriso et al., 2008; Figueira et al., 2011; Figueira and Freitas, 2013; Freitas et al., 2012a; b; Velez et al., 2014, 2015a; b; Chiesa et al., 2018). Among commercially exploited bivalves, Manila clam Ruditapes philippinarum - synonym Venerupis philippinarum (Adams and Reeve, 1850) plays a major role, exceeding 250,000 tons of production per year (FAO, 2013). Originally distributed in the Indo-Pacific region, it has been introduced in many countries for aquaculture and fisheries (Gosling, 2003), including European Atlantic and Mediterranean coastal waters (Chiesa et al., 2017). In Portugal, the first report dates back to 1984 in Ria Formosa (Algarve), but nowadays it has been reported in many estuarine systems all over the country, including the Tagus and Sado estuaries, the Ria de Aveiro and Óbidos lagoons (Gaspar, 2010; Chainho, 2014; Chainho et al., 2015; Velez et al., 2015a; b).

In order to study the complex equilibrium of metal(loid)s in a transitional environment, a holistic approach on a local scale is required for evaluating the element partitioning, dynamics and accumulation in abiotic and biotic matrixes. This approach would be particularly useful to understand the dynamics regulating the bioaccumulation patterns in edible bivalves, specifically Manila clams, exploited from the Ria de Aveiro Lagoon.

Thus, the aims of the present work are multiple: (i) to determine the total metal(loid) content and their partitioning in the estuarine sediments where Manila clam is occurring; (ii) to determine the metal(loid) bioaccumulation in clams; (iii) to identify the driving forces in their biogeochemical dynamics and (iv) their interactions at local scale.

Section snippets

Study area

The Ria de Aveiro Lagoon is located in NW Portugal (40°38′ N, 8°45′ W). It is 45 km long and 10 km wide and covers an area of 83 km2 at high tide (spring tide), reduced to 66 km2 at low tide (Dias et al., 1999). It is characterized by several channels (S. Jacinto, Ílhavo, Mira, Ovar, and Murtosa) and significant intertidal zones, namely mud flats and salt marshes (Dias et al., 2000).

The Ria de Aveiro comprehends a wide range of biotopes (e.g. wetlands, salt marshes and mudflats) used as nursery

Physico-chemical characteristics

Sediment characteristics are fully described in Table 1.

Salinity ranged between 3.6 g/L (ÍL A) and 14.9 g/L (ÍL C), whilst temperature ranged from 19.5 (TR C) to 21.2 °C (TR A).

CN B and TR C showed peculiar characteristics for pH, Eh and total organic matter content (TOM) whose values were always different from the rest of the samples: pH ranged between 6.6 (CN C) and 7.39 (ÍL C), whereas CN B and TR C showed pH values of 7.75 and 7.80, respectively.

Eh ranged from −378 mV (ÍL C) to −45 mV (CN

Sediment characteristics, contamination and geochemistry

The present study demonstrated that, overall, salinity, pH and temperature slightly changed among the sediments of the investigated areas, confirming the previously published studies (Velez et al., 2015a); a high variability for granulometric composition, Eh and TOM content was detected in Costa Nova, Torreira and Ílhavo areas. Differences were observed among, but also within studied areas.

CN B and TR C sites showed sandy granulometric composition, highest Eh values and very low TOM content. On

Conclusions

This study investigated the metal(loid) contamination of sediments and the bioaccumulation patterns of Manila clam from the Ria de Aveiro Lagoon, including for the first time geochemical speciation data. The holistic approach herein applied showed that multiple driving forces interacted together in a complex framework, determining site-specific impacts. These impacts may result in a local risk for the transferring of a determinated metal(loid) from the abiotic to the biotic matrix and

Acknowledgements

Authors would like to thank Cátia Velez (Department of Biology & CESAM, University of Aveiro) for her help with samples collection and field activities.

Funding: Own funds of the Molecular Sciences & Nanosystems Department, Ca’ Foscari University of Venice (Italy). Thanks are also due, for the financial support to CESAM (UID/AMB/50017), to FCT/MEC through national funds, and the co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020.

Silvia Breda benefited from a Ph.D.

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