Sea snail (Hexaplex trunculus) and sea cucumber (Holothuria polii) as potential sentinel species for organic pollutants and trace metals in coastal ecosystems
Graphical abstract
Introduction
The use of sediments or sentinel organisms for environmental assessment is particularly relevant for contaminants with a clear tendency to be transferred to particulate matter (inert of alive). Bivalves are commonly used in international monitoring programmes (UNEP, 1993; OSPAR Commission, 2018) as integrative indicators of the pollution of chemical pollutants in the water column, mainly mussels and oysters. However, these species are not always present or the populations are not useful for monitoring due to their scarcity in some coastal areas and protection, for this reason, alternative invertebrates, such as gastropods (sea snails, limpets, etc.) or echinoderms (sea cucumbers), could be used as potential bioindicators. Gastropods are commonly used as biomonitors species for organotins through imposex effects, because of its high specificity and its sensitivity in relation to other species and endpoints (Alzieu, 1996; Garaventa et al., 2007; Rial et al., 2018). Other studies have considered the use of gastropods as potential metal biomonitors because they have limited mobility (sedentary), they are available all year and easy to sample (Cubadda et al., 2001; María-Cervantes et al., 2008; Reis et al., 2011; Ragi et al., 2017; Pérez et al., 2019), and they take metals from all compartments (i.e. aqueous medium and through ingestion –from food or inorganic particulate material and heavily concentrate them (Phillips, 1977). Particularly, molluscs have limited ability to metabolise PAHs, so it is frequent to detect concentrations of PAHs and persistent organic contaminants (POPs) in different organ tissues (Oehlmann and Schulte-Oehlmann, 2003). However, fewer studies have evaluated the potential use of gastropods as sentinel organisms for the assessment of organic pollution (Storelli et al., 2014; Pérez et al., 2019).
On the other hand, holothurians have been also evaluated as marine bio-indicators, because they also exhibit local-scale migratory movements, they can easily come in contact with all the pollutants of the marine waters as a consequence of these compounds they tend to accumulate in the sediments, place from where the animals extract their food (Parra-Luna et al., 2020). However, these studies were mainly centred in metal contamination (Xin and Chia, 1997; Laboy-Nieves and Conde, 2001; Warnau et al., 2006; Jiang et al., 2014; Mohammadizadeh et al., 2016; Mohsen et al., 2019). Some studies have confirmed the accumulation of organic contaminants such as PCBs (Hope et al., 1997), organochlorine pesticides or PBDEs (Krasnobaev et al., 2020) in some specific areas. Recently validated analytical methods confirmed the occurrence of surfactants, alkylphenols, perfluoroalkyl compounds, triclocarban and parabens in holothurians collected along the coast of Granada (Spain) (Martín et al., 2017). However, less information is available about the accumulation of PAHs in holothurians.
Coastal areas are vulnerable to pollution due to the concentration of activities and population, particularly in semiconfined and shallow areas such as coastal lagoons, being necessary to identify best sentinel species for the monitoring of different groups of contaminants. Mar Menor lagoon (SE Spain) is a hypersaline coastal lagoon affected by heavy seasonal tourist activity, urban development, an intensive agricultural area and metals pollution, mainly in the southeastern area due to mining wastes transferred from abandoned Cartagena-La Unión Sierra (Jiménez-Cárceles et al., 2008; Marín-Guirao et al., 2007). The bioaccumulation of metals has been evidenced for invertebrates, fishes and jellyfishes in several coastal areas (Cubadda et al., 2001; Robinson et al., 2017; Chouvelon et al., 2019; Pérez et al., 2019) and also in the Mar Menor lagoon (Marín-Guirao et al., 2008; María-Cervantes et al., 2008; Muñoz-Vera et al., 2015, Muñoz-Vera et al., 2016; Romero et al., 2020). The concentrations of metals increased in sediments sited close to El Beal wadi, the main watercourse from mining areas (María-Cervantes et al., 2008). Unfortunately, those studies offer a limited view of the metal bioaccumulation in this species from the lagoon, considering mainly the most polluted area.
The bioaccumulation of organochlorinated contaminants in cockle was lower than in oyster and noble pen shell in the Mar Menor lagoon (León et al., 2013a), but similar PAHs bioaccumulation levels were detected in the three bivalve species. However, less information is available in relation to mercury and organic contaminants bioaccumulation in sea snail and currently there is no data about the concentrations of contaminants in sea cucumber in this lagoon under author's knowledge, except for pharmaceuticals (Moreno-González et al., 2016). Sea cucumber has been also identified as a potential bioindicator of trace metal pollution from sediments (Warnau et al., 2006; Turk-Culha et al., 2016; Mohsen et al., 2019), but there is less information available about bioaccumulation of organic contaminants.
Biomagnification has been observed in persistent pollutants along the trophic chain, such as metals (Ragi et al., 2017) or organochlorinated pesticides (Borga et al., 2001; Skarphedinsdottir et al., 2010; Byun et al., 2013). In this sense, other study supported Hexaplex trunculus can be an acceptable sentinel organism to monitor Zn, As, Cd, Mn and Pb (María-Cervantes et al., 2008). However, a previous study has shown that biomagnification does not occur considering different species and trophic levels (stable isotopes C and N content) in two areas from Mar Menor lagoon (Marín-Guirao et al., 2008), although the specific relationship between predator-prey was not adequately estimated and the concentrations in Hexaplex trunculus were two times higher than in cockle for Zn, Cu and Cd. Consequently, it is necessary to confirm if sea snail and sea cucumber can be useful as sentinel not only for metals but also for organic contaminants, being relevant for sea snail due to it is the predominant predator of bivalves in many coastal areas.
Sea snail and holothuria were simultaneously sampled in several areas in spring and autumn to evaluate seasonal variations which can be particularly relevant in a shallow coastal lagoon. Specifically, the bioaccumulation of metals (As, Cd, Cu, Hg, Pb and Zn), polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs) and organochlorinated pesticides (OCPs) in sea cucumber (Holothuria polii) and sea snail (Hexaplex trunculus) from Mar Menor lagoon were characterised. These species of marine invertebrate have different biology which could affect the bioaccumulation and impact of the pollutants. Their influence on the bioaccumulation was studied through the relationship between the levels found in sediment and holothuria, as well as the biomagnification in sea snails from cockle considering previous data for OCs concentrations for the same sampling campaigns (León et al., 2013a) and determining the concentrations of trace metals also in cockle as a novel contribution of this study. Consequently, the main goal of this study is to assess if sea snail (Hexaplex trunculus) and sea cucumber (Holothuria polii) are useful as sentinel species for organic pollutants and trace metals in Mediterranean coastal ecosystems.
Section snippets
Study area and sampling procedure
Sea snails (Hexaplex trunculus) and sea cucumber (Holothuria polii) were sampled in nine areas in the Mar Menor lagoon (Fig. 1), the first three in the north with highest Mediterranean influence, then three in the southern area subjected to a higher mining residue influence and confinement and the final three in the intermediate zone with the highest surface waters inputs. Sea cucumber is sediment deposit feeder and consequently, it is exposed to accumulated pollution in sediment, but it is
Levels of pollutants in sea snail and sea cucumber
This study provides the first data about the distribution of Hg, PCBs, organochlorinated pesticides (OCPs) and PAHs in sea snail (Hexaplex trunculus) and sea cucumber (Holothuria polii) from Mar Menor lagoon. It also characterises the distribution of As, Cd, Pb, Zn and Cu, in sediment, cockle, sea snail and sea cucumber in the whole lagoon. The highest concentrations in sea snail were found for Zn, As, Pb and Cu, followed by Cd, Hg, DDXs, PAHs and PCBs (Table 2, Table 3). However, the highest
Conclusions
The bioaccumulation of contaminants is related to the properties of the marine habitat of the different areas of the study, specific biology, the presence of important sources of pollution or the nature of the pollutants. One of the aims of this study was to determine if the studied species present a similar bioaccumulation patterns and their capacity to be used as bioindicator of the sources of pollution. In the Marine Strategy Framework and Water Framework directives context, the
CRediT authorship contribution statement
V.M. León: Conceptualization, Methodology, Writing – original draft, Writing – review & editing, Supervision, Investigation, Project administration, Funding acquisition. R. Moreno-González: Validation, Formal analysis, Data curation, Writing – review & editing. V. Besada: Methodology, Validation, Data curation, Supervision. F. Martínez: Validation, Formal analysis. C. Ceruso: Formal analysis. V. García: Validation, Formal analysis. F. Schultze: Validation, Formal analysis. J.A. Campillo:
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.
Acknowledgement
This work has been supported by the Spanish Inter-Ministerial Science and Technology Commission and by the European Union through the European Regional Development Fund (ERDF) through ‘DECOMAR’ (CICYT, CTM2008-01832) and PLAS-MED projects (CTM2017-89701-C3-3-R), and by Seneca Foundation (Region of Murcia, Spain) through ‘BIOMARO’ project (15398/PI/10).
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