MERCURY POLLUTION IN COASTAL SYSTEMS: A COMPARATIVE ASSESSMENT USING THE NATIVE OYSTER CRASSOSTREA RHIZOPHORAE AND THE INVASIVE SACCOSTREA CUCCULLATA

Abstract  

The contamination of aquatic ecosystems by toxic elements such as mercury has become a major concern due to increased pollutant emissions. This study aimed to identify oyster species through molecular analysis in three bays of Rio de Janeiro and analyze total mercury concentrations in the native oyster Crassostrea rhizophorae and invasive Saccostrea cuccullata. Results showed higher mercury levels in both species in Ribeira Bay, likely due to its physicochemical conditions. C. rhizophorae consistently accumulated more mercury than the invasive species, suggesting species-specific differences in detoxification. A negative correlation was observed between condition index and mercury concentration, especially in C. rhizophorae. These findings indicate that mercury may influence competition dynamics between native and invasive oysters, with potential ecological and public health implications.

Introduction

The pollution of costal marine environments has intensified in recent decades, being attributed to global population growth and the subsequent increase in pollutant emissions. Among the pollutants, metals are concerning due to their toxicity,persistence, and bioaccumulation. Contamination is generally assessed by analyzing the accumulated metal concentrations found in tissues of biomonitors, characterized as species that can bioaccumulate different pollutants and reflect the environmental changes on water quality efficiently (Boening 1999, Hedge et al. 2009, Wanick et al. 2012). In bivalves, metal concentrations vary between species and individuals from the same locality due to each species-specific capacity to regulate or accumulate trace metals (Otchere et al. 2003). Therefore this study aimed to contribute to the literature on mercury contamination in three bays of Rio de Janeiro, which exhibit rather different levels of mercury input and distinct physicochemical characteristics that influence metal bioavailability, by using two bivalves’ species. Additionally, it aimed to assess potential differences in mercury bioaccumulation between species occupying the same trophic level and similar ecological niche. In particular, it seeks to identify bioaccumulation differences that may indicate different sensitivities of the native and invasive species to mercury exposure, which could consequently increase the dominance of the invasive species due to selective pressures imposed by contamination.

Experimental

For this study, three coastal ecosystems were chosen according to their mercury pollution degrees: Guanabara, Sepetiba and Ribeira bays (Fig. 1). In January 2024, 20 individuals of each species were sampled at each sampling site. In the laboratory, firstly each oyster was photographed individually with its representative label, in order to establish a later connection with the molecular analyses. Molecular identification was performed using a restriction fragment length polymorphism (RFLP) system in conjunction with polymerase chain reaction (PCR) as described by Melo et al. (2010). The amplified genes were 16s and ITS-2, and the restriction enzyme used was haeIII. Total Hg determination was performed on oyster’s samples using a Direct Mercury Analyzer DMA-80 (Milestone, Bergamo, Italy). Triplicates of each sample were performed. Before each sample analysis, blank values were verified to be always less then 0.001 Hg (ng). The results of the mercury (HgT) quantification were expressed as ng·g⁻¹  on a dry weight basis. The accuracy of the results was evaluated and confirmed by the analysis of certified material. Certified samples were analyzed every 10 replicates, with an acceptable error of 10%. A physiological condition index, based on biometric parameters was also used to evaluate effects of environmental stresses. All statistical analyses were conducted in R with a significance level of α = 0.05. Results of the quantification of mercury in oyster tissue and condition index (CI) were treated and analyzed statistically through a Generalized Linear Model (GLM) with the fixed factors: (i) biometric data of oysters, (ii) sites and (iii) species.

Results and Discussion

Firstly, molecular analyses using the PCR-RFLP method were conducted to confirm the identity of the target species. Thus, with the previous morphological analyses and the subsequent molecular methodology, it was possible to reliably separate Crassostrea rhizophorae (native) and Saccostrea cucculata (invasive). The variation in mercury concentrations between the two oyster species across the three studied bays is shown in Figure 2. Mercury concentrations in the oyster Saccostrea cucullata were significantly higher in Ribeira bay compared to Guanabara bay (t = -7.357, p < 0.001) and Sepetiba bay (t = -7.456, p < 0.001). Mercury concentrations in the oyster Crassostrea rhizophorae (were also significantly higher in Ribeira bay compared to Guanabara Bay (t = -6.416, p < 0.001) and Sepetiba bay (t = -8.580, p < 0.001). However, mercury concentrations in the oyster Crassostrea cucculata are higher in all three bays (Fig.2). The GLM results indicate that the invasive oyster has significantly lower mercury concentrations (t = - 6.75, p < 0.001) compared to the native oyster. A linear model was applied to evaluate the condition index (dry weight/wet weight) as a function of the three bays. The analysis showed that oysters from the Ribeira bay have a significantly lower CI compared to those from Sepetiba bay (t = 3.149, p < 0.001) and Guanabara bay (t = 6.164, p < 0.001). When analyzed separately by bays, the decline in CI for both species is significantly associated with increased mercury concentrations in Guanabara and Ribeira bays, however it is not observed in Sepetiba bay. Furthermore, the CI of both species across the three bays shows proportionality, with Crassostrea rhizophorae (native) exhibiting the lowest CI in all three bays (Fig. 3).

Based on observational data and subsequent molecular analyses from the present study, the majority of oysters present in the three bays of the study were the invasive species S. cuccullata, with a significantly higher proportion compared to Crassostrea rhizophorae. Native oyster banks have declined in abundance in more then 70% of “bays” (bays, estuarines, embayments, coastal counties, and portion of coastines) worldwide (Beck et al. 2011). The results indicate that HgT is more bioavailable in Ribeira bay, however, its highest input of mercury occurs in Guanabara and Sepetiba bay (Rodrigues, 2010). That is despite the higher mercury input in Guanabara and Sepetiba bays, the highest mercury concentrations in oysters from both species were found in Ribeira bay, suggesting that this bay higher mercury bioavailability due to its physicochemical characteristics. These results highlighted the possibility of using these two species as biomonitors of mercury bioavailability in coastal systems. However, although the pattern was similar between species, mercury concentrations were higher in the native oyster across all bays. The fact that Crassostrea rhizophorae (native) exhibits higher mercury concentrations than Saccostrea cuccullata (invasive) suggests that these two species may have distinct mechanisms for accumulating and/or detoxifying the metal. The condition index (CI) used indicated that oysters from both species in Ribeira Bay (where the highest mercury concentrations in oysters were found) had the lowest condition index among the three bays. Additionally, the native oyster (which had the highest mercury concentrations) exhibited a lower CI across all three bays when compared to the invasive Saccostrea cuccullata.

Conclusions

This study highlights the importance of understanding mercury effects and tolerance in native and invasive oyster species. The observed differences in bioaccumulation suggest that environmental contamination may modulate competitive dynamics between species, potentially favoring the invasive oyster. Continuous monitoring of mercury in bivalves is essential for evaluating contamination patterns and their ecological implications in coastal ecosystems.