Mercury
The total Hg in the soft tissue of S. palmula and C. corteziensis ranged from 0.03–0.16 and 0.02–0.17 µg g−1 (wet weight), respectively. In relation to other studies in Mexico, the Hg concentrations are similar to those obtained in this study (Table 5), but lower than those found for C. virginica in the Términos lagoon (Gulf of Mexico), mainly affected by oil, agricultural and urban activities (Aguilar et al. 2012).
Table 5
Total mercury range concentrations (µg g−1 ww) in different oyster species from some coastal lagoons of NW Mexico and other worldwide regions
Species | Area (sampling year) | Total Hg | Author |
Coastal lagoons of NW Mexico |
C. gigas | Coastal waters, Sonora (1997) | 0.01–0.06 | García-Rico et al. (2001) |
C. gigas* | Guaymas Bay, Sonora (NA) | 0.04** | Green-Ruiz et al. (2005) |
C. corteziensis* | Urías lagoon, Sinaloa (2006) | 0.006–0.01 | Jara-Marini et al. (2008) |
C. corteziensis | Bacochibampo Bay, Sonora (2004–2005) | 0.03–0.04 | García-Rico et al. (2010) |
C. corteziensis* | Coastal lagoons, Sinaloa (NA) | 0.03–0.11 | Osuna-Martínez et al. (2010) |
C. gigas* | Coastal lagoons, Sinaloa (NA) | 0.01–0.18 | Osuna-Martínez et al. (2010) |
C. virginica* | Términos lagoon, Campeche (NA) | 0.08–0.40 | Aguilar et al. (2012) |
C. virginica* | Northern Gulf of Mexico, USA (NA) | 0.006–0.10 | Apeti et al. (2012) |
C. corteziensis* | Tobari lagoon, Sonora (2009) | 0.07–0.10 | Jara-Marini et al. (2013) |
Crassostrea spp.* | Coastal lagoons, Sinaloa-Nayarit (2010–2011) | 0.02–0.05 | Delgado-Alvarez et al. (2015) |
S. palmula* | Coastal lagoons, Sinaloa (2008–2009) | 0.04–0.15 | Páez-Osuna and Osuna-Martínez (2015) |
C. corteziensis* | Coastal lagoons, Sinaloa (2008–2009) | 0.03–0.12 | Páez-Osuna and Osuna-Martínez (2015) |
C. gigas | La Pitahaya estuary, Sinaloa (2011) | 0.003–0.04 | Góngora-Gómez et al. (2017) |
C. gigas | Navachiste lagoon, Sinaloa (2011–2012) | 0.003–0.03 | Jonathan et al. (2017) |
C. gigas* | Coastal lagoons, Sinaloa (2013–2014) | 0.03–0.14 | Muñoz-Sevilla et al. (2017) |
C. corteziensis* | Urías lagoon, Sinaloa (2012–2013) | 0.01–0.05 | Frías-Espericueta et al. (2018) |
C. gigas | Coastal waters, Sonora (2010) | 0.01–0.13 | García-Rico and Tejeda‑Valenzuela (2018) |
S. palmula | Coastal lagoons, Sinaloa (2019–2020) | 0.03–0.16 | This study |
C. corteziensis | Coastal lagoons, Sinaloa (2019–2020) | 0.02–0.17 | This study |
Other worldwide regions |
C. gigas* | Minamata Bay, Japan (NA) | 2.00** | Eisler (1987) |
C. rhizophorae* | Channel of Santa Cruz, Brazil (1993–1994) | 0.05–0.44 | Meyer et al. (1998) |
C. tulipa* | Benya, Ningo lagoons, Ghana (NA) | 0.02–0.04 | Otchere et al. (2003) |
C. rhizophorae* | Gulf of Paria, Venezuela and Trinidad (NA) | 0.002–0.01 | Rojas de Astudillo et al. (2005) |
C. virginica* | Gulf of Paria, Venezuela and Trinidad (NA) | 0.002–0.01 | Rojas de Astudillo et al. (2005) |
C. rhizophorae* | Estuarine systems, Northeast Brazil (NA) | 0.004–0.06 | Vaisman et al. (2005) |
C. gigas | Oualidia lagoon, Morocco (2004–2005) | 0.02–0.21 | Maanan (2008) |
C. rhizophorae* | Villa Clara, Cuba (NA) | 0.03–0.13 | Olivares-Rieumont et al. (2012) |
C. rhizophorae* | Santos and Paranaguá estuaries, Brazil (2008–2009) | 0.02–0.07 | Torres et al. (2012) |
C. gigas* | Ebro Delta in Catalonia, Spain (2008–2009) | 0.02–0.05 | Ochoa et al. (2013) |
C. gigas | Coastal waters, Korea (2009–2013) | 0.006–0.02 | Mok et al. (2015) |
C. gigas | Coastal marine ecosystems, Italy (NA) | 0.01–0.34 | Burioli et al. (2017) |
*Calculated from dry weight, assuming 80% moisture |
**Only the mean value was available. NA not available |
Compared with other regions of the world, the level of Hg obtained in S. palmula and C. corteziensis is similar to those reported for C. gigas and C. rhizophorae in Morocco (Maanan 2008) and Cuba (Olivares-Rieumont et al. 2012), but higher than those determined for C. rhizophorae in the Santos and Paranaguá estuary, Brazil (Torres et al. 2012), for C. gigas in the Ebro Delta in Catalonia, Spain (Ochoa et al. 2013) and for C. virginica and C. rhizophorae in the Gulf of Paria, Venezuela and Trinidad (Rojas de Astudillo et al. 2005). However, the Hg concentration in this study was lower than those recorded for C. gigas in Minamata Bay, Japan (Eisler 1987) and in some coastal and marine regions of Italy where the Japanese oyster is cultivated (Burioli et al. 2017) (Table 5). These differences could be due to the abundance of Hg in the continental crust (on mean it is higher than 0.056 µg g−1), since the level of Hg in the world is not homogeneous and some regions are more enriched than others (Wedepohl 1995; Rytuba 2003). Also, Hg concentration can vary among oyster species due to biological aspects, related to their metabolic activity, differences between sizes, and reproductive period (Páez-Osuna et al. 1995; Frías-Espericueta et al. 2009).
The bioaccumulation of Hg in S. palmula and C. corteziensis could be due to their benthic and feeding habits, since they filter large volumes of seawater (around 10 to 20 L min−1) through the cilia, mantle and gills (Mazón-Suástegui et al. 2009; Shenai-Tirodkar et al. 2016), where the metal is suspended (Aguilar et al. 2012; Jonathan et al. 2017). Mercury is one of the most persistent chemical elements and can be distributed and accumulated in various tissues and organs of aquatic organisms; eventually, it can be biomagnified from lower trophic levels to humans (Burioli et al. 2017; Murillo-Cisneros et al. 2021). Oysters live mainly attached to the roots of mangroves (i.e. Rhizophora spp.) and on rocky surfaces, exposed and/or buried in muddy sediments (Lodeiros et al. 2020) with a high content of organic matter, which favors retention of metals, such as Hg (Aguilar et al. 2012; Rangel-Peraza et al. 2015; Navarrete-Rodríguez et al. 2020). Therefore, it is possible to infer that the sediments in the study area could be one of the most important routes of Hg accumulation in these bivalves (Sepúlveda et al. 2020).
The annual mean concentration of Hg in both oyster species did not show significant differences (p ˃ 0.05) among the sampling sites (Table 3), which could be partially explained by the natural and continuous contribution of leaching from the soils-rocks and by waste from the mining industry (key source of Hg). It has been reported that such wastes are transported along rivers and streams that originate in the Sierra Madre Occidental (an area rich in minerals) and, eventually, end up in the coastal lagoons of NW Mexico at low concentration (Murray and Busty 2015; Gamboa-García et al. 2020). During the colonial period until the beginning of the 20th century, the mining industry used approximately 200,000 t of Hg in the silver and gold extraction process, and it is estimated that just under half of that used Hg is still present in mining tailings (Delgado-Alvarez et al. 2015; Niane et al. 2019). The Hg used by the mining activity in the state of Sonora (the main gold producer in Mexico), is transported atmospherically to the coastal lagoons of NW Mexico and accumulated in the sediments and different trophic levels (Ruelas-Inzunza et al. 2008); in this way, its impact could reach areas with a low contamination level far from its sources of origin (Apeti et al. 2012; Kakimoto et al. 2019). In addition, Hg levels in coastal lagoons may increase due to upwelling events and the continuous renewal of seawater (Páez-Osuna and Osuna-Martínez 2015). Another important source of this metal is the effluents from intensive agriculture in NW Mexico, since Hg-based fungicides are still used to control pests of various crops (Osuna-Martínez et al. 2010). Mercury can also reach lagoons due to various causes such as: continental runoff, untreated wastewater treatment systems, paint waste, batteries, cement plant waste, and dental objects (Frías-Espericueta et al. 2014).
Regarding the seasonal influence, Osuna-Martínez et al. (2010), Páez-Osuna and Osuna-Martínez (2015) and Muñoz-Sevilla et al. (2017) reported higher concentrations of Hg in C. gigas, C. corteziensis, and S. palmula during the rainy season (summer–autumn), which were related to continental runoff from the vast agricultural areas that reach the coastal lagoons with increased wet deposition. Frías-Espericueta et al. (2018) reported significantly higher concentrations of Hg in C. corteziensis collected in the Urías lagoon (NW Mexico) in November 2012 (autumn). In this study, a similar trend occurs, since the Hg level in both oyster species was significantly higher (p < 0.05) during summer–autumn 2019 (rainy season) (Table 2). On the other hand, García-Rico et al. (2010) did not observe significant differences in the seasonal Hg concentration in C. gigas, probably due to the continuous contribution of anthropogenic activities in Bacochibampo Bay, Sonora.
Despite the natural sources and anthropogenic activities that contribute with Hg deposition in the coastal lagoons of NW Mexico, the Hg concentration in S. palmula and C. corteziensis was below the maximum permissible limit of 1.0 (µg g−1, wet weight) established by the Mexican legislation (Norma Official Mexicana NOM-031-SSA1-1993), the World Health Organization (WHO 1982), and the United States Food and Drug Agency (FDA 2006), which indicates that the consumption of these species from the sampled lagoons does not represent a risk to human health with respect to Hg poisoning.
Selenium
Information about the effect of Se on oysters is scarce. Okazaki and Panietz (1981) reported that the level of this metalloid was higher than that of Hg, in different tissues (mantle, gill and digestive gland) of C. gigas and C. virginica, from San Francisco Bay (California, USA), which agrees with the present study. However, the concentration of Se reported by these authors is lower than those determined in S. palmula and C. corteziensis (Table 2). This could be due to factors such as the bioavailability of this element in coastal lagoons, as well as the sizes and stages of the organisms (Jara-Marini et al. 2008; Ochoa et al. 2013). The annual mean concentration of Se for S. palmula (3.34 ± 0.96 µg g−1) and C. corteziensis (2.79 ± 0.89 µg g−1) was significantly (p < 0.05) higher in ECL9 (Table 3). This site is located in one of the most contaminated areas by metals and metalloids within the El Colorado lagoon (Páez-Osuna and Osuna-Martínez 2015), which is part of the Agiabampo-Bacorehuis-Río Fuerte Antiguo lagoon system and, which, receives the contributions of the Fuerte River and the runoff from the highly technical agricultural activities of the municipality of Ahome (~ 189,064 ha; SIAP 2019), municipal waste (~ 459,310 inhabitants; INEGI 2020) and shrimp farms (~ 12,639 ha; CESASIN 2019) (Cárdenas 2007). Navarro-Alarcón and Cabrera-Vique (2008) and Santos et al. (2015) mention that the aquatic environment can be contaminated by Se due to agriculture, urban drainage, mining waste, thermoelectric plants, oil refineries and metallic minerals.
In the case of S. palmula and C. corteziensis collected from the same mangrove roots in sites AL2, ML5, NL6, NL8 and ECL9 (Fig. 1), we hypothesized that the total Hg and Se concentrations were similar between both species, probably because the oysters were under the same water conditions and exposure levels. As expected, there was no significant difference with the concentrations of the study elements between the oysters (p ˃ 0.05). These results may be useful in the intercomparison of Hg and Se levels among different sites involving S. palmula and C. corteziensis, as mentioned by Páez-Osuna and Osuna-Martínez (2015) for the same species and lagoons of sampling. Similar observations were recorded by Osuna-Martínez et al. (2010) for C. gigas and C. corteziensis grown in the Ceuta lagoon, Sinaloa.
Mercury and selenium: influence of the size, weight and condition index in oysters
According to Trudel and Rasmussen (2006), there is a direct correlation between the Hg content and the age or body size of aquatic organisms, due to the greater exposure of the metal, which is excreted more slowly as it is ingested. Acosta and Lodeiros (2004) reported that the highest concentrations of metals were proportionally related to the shell size of the clam Tivela mactroides. However, Collaguazo-Collaguazo et al. (2017) reported that small clams Anadara tuberculosa have the ability to bioaccumulate a higher concentration of metals (including Hg) than large clams. In addition to the species and the level of exposure, other physiological factors such as spawning and body size of bivalves, can influence the accumulation and variability of metals and metalloids in their tissues (Aguilar et al. 2012; Muñoz-Sevilla et al. 2017). In this study, specimens of S. palmula and C. corteziensis of similar sizes (72.15 ± 4.95 and 73.57 ± 5.31 mm, respectively; Table 1) were collected to reduce possible variations in the level of metals due to the size of the organisms. However, their body weight varied significantly with the seasons, which suggests that these values could be associated with reproductive cycle, as reported by Rodríguez-Jaramillo et al. (2008) and Góngora-Gómez et al. (2020) for C. corteziensis. This pattern has also been observed in other ostreids such as C. rhizophorae (Rebelo et al. 2005), C. gigas and C. corteziensis (Osuna-Martínez et al. 2010), C. virginica (Aguilar et al. 2012), C corteziensis and S. palmula (≈ Crassostrea palmula) (Páez-Osuna and Osuna-Martínez 2015). In fact, the Hg concentration in S. palmula was slightly correlated with CI (rp = –0.29, p < 0.05), which agrees with that reported by Osuna-Martínez et al. (2010) for C. gigas cultivated in the coastal lagoons of NW Mexico.
Se/hg Molar Ratio And Health Benefit
It has been documented that Se can neutralize the toxic effect of Hg, as long as it’s Se/Hg molar ratio is > 1 (Burger and Gochfeld 2013). Selenium intervenes in the Hg demethylation process through the selenocysteine protein, transforming the metal to its inorganic and less toxic form (Escobar-Sánchez et al. 2010; Vega-Sánchez et al. 2020); this way, Hg can be excreted more easily through pseudofeces and spawning (Rodríguez de la Rua et al. 2005; Havelková et al. 2008). The present study reports for the first time the Se/Hg molar ratio in S. palmula and C. corteziensis in NW Mexico, inclusive, in the distribution area of these two species (Pacific coast from Mexico to Peru; Lodeiros et al. 2020). The Se/Hg ratio was always greater than 1 in both species of oyster, which can be explained by the low level of Hg found (Burger and Gochfeld 2013). These results are similar to the Se/Hg ˃ 1 molar ratios found in different groups of organisms, as in shrimps Farfantepenaeus californiensis and Litopenaeus stylirostris (NW of Mexico) (Frías-Espericueta et al. 2016), the mahi mahi fish Coryphaena hippurus (Gulf of California) (Bergés-Tiznado et al. 2019), Pacific hake Merluccius productus (Gulf of California) (Acosta-Lizárraga et al. 2020), crustaceans like the crab Callinectes arcuatus (NW of Mexico) (Delgado-Alvarez et al. 2020), and elasmobranchs like the shark Mustelus henlei (Mexican Pacific Ocean) (Medina-Morales et al. 2020). Regarding the value of the health benefit by Se, calculated through the HBVSe index obtained for S. palmula and C. corteziensis among the sampling sites (Table 3), it indicates a benefit provided by a higher concentration of Se in comparison to Hg in the soft tissue of oysters. Similar observations were recorded for fishes Thunnus albacares, Vinciguerria lucetia, Lagocephalus lagocephalus; squids Dosidicus gigas, Thysanoteuthis rhombus, Sthenotheuthis oualaniensis and the crab Pleuroncodes planipes (HBVSe = 64.54, 19.41, 298.40, 12.82, 30.30, 63.52 and 13.26, respectively; Ordiano-Flores et al. 2012); as well as for sharks Carcharhinus falciformis (HBVSe = 52.30; Bodin et al. 2017), and fish C. hippurus (HBVSe = 1.77; Vega-Sánchez et al. 2020).
Health Risk Assessment
Recent studies highlight the importance of evaluating the potential risk to human health from the ingestion of metals and metalloids contained in commercially important fishery products (including oysters). This is done to identify populations at risk, especially in cities and coastal communities dedicated to the capture and production of seafood, where specifically, the annual consumption of oysters is double or more (Delgado-Alvarez 2015) than established as national apparent consumption (0.39 kg/year; CONAPESCA 2017). In the case of the present study, the hazard quotient (HQ) values remained below the risk level (HQ < 1); therefore, the ingestion of Hg, MeHg and Se due to the consumption of S. palmula and C. corteziensis does not represent a risk to human health. These results are similar to the studies by Delgado-Alvarez et al. (2015), Frías-Espericueta et al. (2018), and García-Rico and Tejeda-Valenzuela (2018), who reported HQ values below 1, in Crassostrea spp. (Sonora-Nayarit lagoons), C. corteziensis (Urías lagoon, Sinaloa), and C. gigas (Sonora lagoons), respectively. However, as a precautionary measure, it is important to consider both the frequency of consumption of oysters and the amount of organisms consumed, since Hg levels (above the limits of established legislation) can involve health risks, mainly to vulnerable people (children, pregnant women and/or malnourished people) (Taylor et al. 2014).