Elsevier

Food Control

Volume 118, December 2020, 107368
Food Control

Revealing the illegal harvesting of Manila clams (Ruditapes philippinarum) using fatty acid profiles of the adductor muscle

https://doi.org/10.1016/j.foodcont.2020.107368Get rights and content

Highlights

  • Fatty acid (FA) profiles of the adductor muscle trace the harvesting site of Manila clams .

  • The dominant FAs were the 22:6n-3 (DHA), 16:0 (PA) and 20:5n-3 (EPA).

  • Collection site of Manila clams with unknown origin was pinpointed.

  • The illegal harvesting of Manila clams from interdicted areas was uncovered.

Abstract

The Manila clam (Ruditapes philippinarum) is one of the most traded bivalves in the world. Knowing its harvesting location is therefore paramount to guarantee the safety of consumers. The present study employs fatty acid (FA) profiles of the adductor muscle (AM) to reveal the most likely harvesting location of four batches of Manila clams suspected of having been illegally sourced from the Tagus estuary. In this ecosystem, where the collection of Manila clams is currently prohibited for food safety reasons, illegal, unreported and unregulated (IUU) capture is known to occur. In order to trace the geographic origin of these four batches of Manila clams, a reference model based on the FA profiles of the AM was developed with specimens originating from the two most representative ecosystems supplying the trade-chain of this species in mainland Portugal (the Tagus estuary and Ria de Aveiro), as well as Ría de Vigo, a production area outside Portugal and that is also an important supplier. The ability of this model to allocate clams to its origin ecosystem was evaluated using independent datasets, with an allocation success of 100% (all samples were correctly assigned to its origin ecosystem, thus validating the model). Based on the reference model established, the harvesting location of the four batches suspected of originating from ongoing IUU in the Tagus estuary was investigated. Specimens from 3 of the 4 batches screened were classified, as most likely originating from the Tagus estuary (with a likelihood ranging from 90% up to 100%). These results highlight the potential of this approach to fight the IUU capture of Manila clams, as this practice endangers important habitats and threatens public health.

Introduction

Marine bivalves, such as oysters, mussels, cockles and clams are among the most consumed seafood products worldwide. The Manila clam (Ruditapes philippinarum) is one of the most representative of such bivalves, with a production in 2017 of over 35.000 tons in Europe alone (FAO, 2019). Native from South-east Asia (Indo-Pacific), R. philippinarum is an invasive species in European coasts (Humphreys et al., 2015), where it was introduced in the early 1970's. In Iberian Peninsula, this species has been reported since late 1980's (Campos & Cachola, 2005; Chiesa et al., 2017), presenting currently well-stablished populations which turned it an important economic resource in this area (FAO, 2019).

Despite their high nutritional value, bivalves can at times threaten human health. Due to their suspension feeding nature, bivalves can accumulate pathogenic bacteria, being this especially dangerous for human health if consumed raw or lightly cooked (Cook, 1991, pp. 19–39; Wright, Fan, & Baker, 2018), as well as metals and metalloids present in the water (Karouna-Renier, Snyder, Allison, Wagner, & Ranga Rao, 2007; Velez, Figueira, Soares, & Freitas, 2015). These issues are related with water and sediment quality of the harvesting location (Li, Yu, Song, & Mu, 2006; Stabili, Terlizzi, & Cavallo, 2013). In order to safeguard public health, the European Union (EU) already produced several pieces of legislation (Regulation (EC) No 853/2004, No 854/2004, No 2073/2005 and No 1021/2008) classifying bivalves harvesting areas according to the levels of Escherichia coli they display per g of bivalves flesh and intravalvular liquid (EC, 2004a; 2004b, 2005, 2008). Moreover, to ensure the traceability of each batch of seafood traded in the European Union, it also stablished several labelling regulations (Regulation (European Commission (EC)) No 104/2000 and No 1224/2009; Regulation (EU) No 404/2011 and No 1379/2013) (EC, 2000, 2009; EU, 2011, 2013). The more recent and demanding of these labeling regulations (Regulation (EU) No 1379/2013) (EU, 2013) stipulates, among other specifications, that marketed seafood products need to display the catch area, production method and fishing gear used. In this way, the development of traceability tools for origin certification is paramount to avoid seafood mislabeling, being key to ensure safety for human consumption (Leal, Pimentel, Ricardo, Rosa, & Calado, 2015; Moretti, Turchini, Bellagamba, & Caprino, 2003).

Environmental factors, such as temperature, salinity and sediment type, influence the spatial distribution of bivalves (Gosling, 2003) modulating their fatty acids (FA) profile (Calado & Leal, 2015). For instance, high salinity fluctuations and low temperatures influence the structure and fluidity of cell membranes. This results in a lower saturated FA (SFA) content, that stabilize bilayer cellular membranes, with these biomolecules being replaced by polyunsaturated FA (PUFA), which allow higher membrane fluidity (Fokina, Ruokolainen, Bakhmet, & Nemova, 2015; Nemova, Fokina, Nefedova, Ruokolainen, & Bakhmet, 2013). Other driving factor of the FA composition in bivalve tissues is trophic history, with the predominance of certain FA revealing their dietary regimes (Calado & Leal, 2015; Prato, Danieli, Maffia, & Biandolino, 2010). The FAs 16:0, 16:1n-7 and 20:5n-3 (eicosapentaenoic acid, EPA) in bivalves tissues reveal the consumption of diatoms, while PUFA 18:3n-3 and 18:2n-6 of green microalgae, 22:6n-3 (docosahexaenoic acid, DHA) and 18:4n-3 of dinoflagellates, and odd chain FA (15:0 and 17:0) and 18:1n-7 of detritus/bacteria (among others, Calado & Leal, 2015; Dalsgaard, John, Kattner, Müller-Navarra, & Hagen, 2003; Ezgeta-Balić, Najdek, Peharda, & Blažina, 2012; Fujibayashi, Nishimura, & Tanaka, 2016; Nerot et al., 2015). These indicative features allow to apply the profiling of FA signatures of tissues from different marine species for multiple scopes, such as identifying their feeding habitats (e.g. Coelho et al., 2011; Xu, Xu, Zhang, Peng, & Yang, 2016), diet composition (e.g. Bosley, Copeman, Dumbauld, & Bosley, 2017; White et al., 2017), seasonal variations in dietary habits (e.g. Soler-Membrives, Rossi, & Munilla, 2011) or trace their geographic origin (Ricardo et al., 2015; Ricardo, Maciel, Domingues, & Calado, 2017; Zhang, Liu, Li, & Zhao, 2017).

The FA profile of the adductor muscle (AM) proved to be suitable in geographic origin traceability studies targeting diverse bivalve species, such as cockles (Cerastoderme edule; Ricardo et al., 20157, 2015), scallops (Pecten maximus; Grahl-Nielsen, Jacobsen, Christophersen, & Magnesen, 2010) and clams (Astarte sulcata; Olsen, Grahl-Nielsen, & Schander, 2009). The AM is of particular interest in traceability studies, mainly due to its high content in polar lipids, which prevents short-term turnover in the FA profile related to dietary shifts (Grahl-Nielsen et al., 2010; Leal et al., 2015; Olsen et al., 2009).

To avoid the fraudulent mislabeling of seafood geographic origin, it is important to develop and refine traceability tools. Therefore, the present study aimed to develop a model based on the FA profile of the AM that could indicate the most likely harvesting location of four batches of R. philippinarum suspected of having been illegally harvested from the Tagus estuary (where the harvesting of Manila clams is forbidden due to food safety issues). A two-step approach was employed to develop this model: i) Manila clam samples harvested from three ecosystems (the Tagus estuary and Ria de Aveiro, two Portuguese ecosystems that supply ~95% of the whole Manila clam traded in Portugal, and Ría de Vigo, a Spanish ecosystem that is also an important supplier of this species to the Portuguese market) were used to validate a predictive model to trace their geographic origin; and following the validation of the predictive model ii) the FA profile of the AM of clams suspected of originating from the Tagus estuary were screened to verify if these clams had indeed been harvested in this area where their capture is illegal.

Section snippets

Study areas and clam collection

Thirty specimens of R. philippinarum were collected in May 2018 in the Tagus estuary (Te, Portugal), Ria de Aveiro (RAv, Portugal) and Ría de Vigo (RV, Spain) (3 ecosystems X 30 replicates = 90 samples; Fig. 1). These ecosystems play an important role in the Portuguese trade of R. philippinarum, with these clams being intensively harvested in these locations. However, it must be highlighted, that regardless of the Tagus estuary being the main source of Manila clams supplying the Portuguese

Results

The mean relative abundance of each FA per sampling group is presented in Table 1. A total of 26 FAs were identified, being HUFA the most dominant class (50–53%), with eicosapentaenoic (20:5n-3; EPA) and docosahexaenoic (22:6n-3; DHA) acids being the most relevant ones, followed by SFA (22–26%), with the predominance of palmitic (16:0; PA) and stearic (18:0) acids. The least represented classes were MUFA (13–18%), mostly present due to oleic (18:1n-9) and eicosenoic (20:1n-9/11) acids, and PUFA

Discussion

The fraudulent mislabeling of geographic origin is a well-known problem in the seafood trade (Leal et al., 2015). The significant differences recorded in the FA profiles of the AM of Manila clams originating from the three ecosystems surveyed in the present study, confirmed the potential of this biochemical tool to trace the geographic origin of bivalves, as already highlighted by previous studies (Grahl-Nielsen et al., 2010; Olsen et al., 2009; Ricardo et al., 2017, 2015).

The FA profile of the

CRediT authorship contribution statement

Renato Mamede: Conceptualization, Methodology, Data curation, Formal analysis, Writing - original draft, Writing - review & editing, Data curation. Fernando Ricardo: Conceptualization, Methodology, Data curation, Writing - review & editing, Project administration. Andreia Santos: Methodology, Writing - review & editing. Seila Díaz: Methodology, Writing - review & editing. Sónia A.O. Santos: Methodology, Writing - review & editing. Regina Bispo: Formal analysis, Writing - review & editing. M.

Declaration of competing interest

The authors declare that they have no conflict of interest.

Acknowledgements

This work was financially supported by project TraSeafood (Tracing the geographic origin of seafood as a pathway towards the smart valorization of endogenous marine resources) (PTDC/BIA-BMA/29491/2017), funded by FEDER, through PT2020 Partnership Agreement and Compete 2020 and by national funds (OE), through FCT/MCTES. This work was also funded by the Integrated Programme SR&TD ‘Smart Valorization of Endogenous Marine Biological Resources Under a Changing Climate’ (Centro-01-0145-FEDER-000018),

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