Bioaccumulation and biochemical patterns of Ruditapes philippinarum clams: Responses to seasonality and low contamination levels
Introduction
Coastal ecosystems, including lagoons and estuaries, are complex systems with high primary production (McLusky, 1999). They have a role of paramount importance in providing several ecosystem services, often associated to the sustenance of vast biological resources (Lillebø et al., 2015). However, these ecosystems are often negatively impacted by natural shifts (Govender et al., 2011) and anthropogenic activities (Langston et al., 2010), including climate change related factors and pollution. Classical environmental monitoring and ecological health status evaluation through water and sediment chemical analysis associated to the evaluation of biological effects upon inhabiting biota are approaches commonly used (WFD 2000/60/EC, 2000) in order to assess negative impacts derived from chemical exposure before it becomes relevant in higher levels of the biological organization (Picado et al., 2007). Environmental monitoring has been based on the effects induced in benthic organisms, by the evaluation of alterations at the community level (benthic community parameters) and, at individual and cellular levels (physiological and biochemical markers), mainly to assess the impacts of pollutants but, more recently, to investigate alterations derived from climate change, especially related with extreme weather events. Cellular alterations are widely described in literature as a response to natural and anthropogenic stressors (Magalhães et al., 2018; Munari et al., 2018; Gonçalves et al., 2017; Velez et al., 2016; Carregosa et al., 2014; Harley et al., 2006). In particular, cellular biomarkers have been used to assess the negative impacts of metals and metalloids (Chiesa et al., 2018, Coppola et al., 2018), temperature (Keller et al., 2004), salinity (Freitas et al., 2015; Moreira et al., 2016) and pH (Velez et al., 2016). Within benthic macrofauna assemblages, clam species are identified as important bioindicators due to their high abundance, filter-feeding habits and socio-economic relevance (reviewed in Bebianno et al., 2004).
The Manila clam (Ruditapes philippinarum, Adams et al., 1850) is a native species from the Indo-Pacific region, introduced in Europe at the beginning of the 1970s for culture purposes (Flassch and Leborgne, 1992; Jensen et al., 2004), becoming a highly exploited resource (Pranovi et al., 2006; Dang et al., 2010). This species is commonly exploited in a wide variety of aquatic systems due to its fast adaption to new environmental scenarios, fast growth and high commercial value (Usero et al., 1997). More recently, R. philippinarum was introduced in Portugal, being currently one of the most widely used bivalve species to assess environmental quality (Breda et al., 2018, Chiesa et al., 2018, Costa et al., 2013; Martín-Díaz et al., 2007; Shin et al., 2002). As an example, Costa et al. (2013) performed histopathological assays in R. philippinarum specimens, aiming to assess the environmental quality of the Portuguese south coast. Studies conducted by Moschino et al. (2012) also demonstrated the capacity of Manila clam as a bioindicator species, revealing the clam's responses to pollutants concentrations along the Venice lagoon (Italy). Nevertheless, under environmental conditions when ecosystem pollution levels are low it is often difficult to determine whether effects are due to pollutants or natural environmental shifts closely linked with the organism's life cycle (Sheehan and Power, 1999; Hook et al., 2014), which can seriously compromise the interpretation of monitoring data. Thus, it is important to understand how the natural variations associated with seasonal changes such as salinity and temperature may impact the inhabiting fauna life cycle and, consequently, can alter the organism's responses to pollutants.
Therefore, the general aim of the present study was to evaluate the capacity of R. philippinarum as a bioindicator species in a low contaminated coastal system along four distinct seasons, testing the hypothesis that pollution levels may hide the effects induced by seasons on the clam's natural biochemical performance. For this, the biochemical performance of R. philippinarum specimens, collected from six different areas along the Ria de Aveiro (Portugal), characterized by different metal(oid)s concentrations, was assessed during four seasons (Winter, Spring, Summer and Autumn). The risk for human health derived from clam's consumption was also evaluated.
Section snippets
Site description
The present study was conducted at the Ria de Aveiro (Fig. 1), a shallow, vertically homogeneous, coastal lagoon located on the northwest coast of Portugal. This aquatic system is 45 km long and 10 km wide, comprising a total surface area of 83 km2 at high tide, with 17 km2 of intertidal flats emerging at low tide (Dias et al., 2000). In addition, this aquatic system is characterized by narrow channels and by large areas of mud flats and salt marshes (Picado et al., 2009).
Sampling was conducted
Environmental parameters
In the present study, the obtained results showed that salinity and water temperature were higher in the Summer compared to the coldest seasons, Winter and Autumn, which presented the lowest values respectively. In warmer seasons, area T presented the highest temperature values, while areas S and CO were the coldest ones. Nonetheless, the lowest water temperature value of this study was recorded during Autumn in area M. Regarding salinity, the highest value was obtained in area T during Summer,
Elements concentrations
In the present study the results obtained showed higher water contamination during Summer, with area CO being the one with the highest values. The seasonal effect upon elements concentration in water column was highlighted in this study, suggesting that higher metal(loids) water levels led to an additional concern about the elements’ bioavailability, particularly during Summer. Generally, higher metal(loids) concentrations in water are related to environmental parameters such as temperature and
Conclusions
The present study highlights the importance of identifying the potential interfering factors and their impacts on the biomarker signals observed in wild populations. Biomarkers can thus, be significantly affected not only by anthropogenic or natural stressors but also by the combined action of both. Moreover, the optimal season for carrying out biomarker field studies or regular monitoring is of utmost relevance and should be investigated prior to including biomarkers in monitoring programs.
In
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
Rosa Freitas and Bruno Henriques were funded by national funds (OE), though Fundação para a Ciência e a Tecnologia (FCT), in the scope of the framework contract foreseen in the numbers 4, 5 and 6 of the article 23 of the Decree-Law 57/2016 of August 29, changed by Law 57/2017 of July 19. This work was also financially supported by the project ASARISAFE – Safety and sustainable management of valuable clam product in Portugal and China funded by the National Funds through the Portuguese Science
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