Contamination and oxidative stress biomarkers in estuarine fish following a mine tailing disaster

Abstract

Background: The Rio Doce estuary, in Brazil, was impacted by the deposition of iron mine tailings, caused by the collapse of a dam in 2015. Based on published baseline datasets, the estuary has been experiencing chronic trace metal contamination effects since 2017, with potential bioaccumulation in fishes and human health risks. As metal and metalloid concentrations in aquatic ecosystems pose severe threats to the aquatic biota, we hypothesized that the trace metals in estuarine sediments nearly two years after the disaster would lead to bioaccumulation in demersal fishes and result in the biosynthesis of metal-responsive proteins.

Methods: We measured As, Cd, Cr, Cu, Fe, Mn, Pb, Se and Zn concentrations in sediment samples in August 2017 and compared to published baseline levels. Also, trace metals (As, Cd, Cr, Cu, Fe, Hg, Mn, Pb, Se and Zn) and protein (metallothionein and reduced glutathione) concentrations were quantified in the liver and muscle tissues of five fish species (Cathorops spixii, Genidens genidens, Eugerres brasilianus, Diapterus rhombeus and Mugil sp.) from the estuary, commonly used as food sources by local populations.

Results: Our results revealed high trace metal concentrations in estuarine sediments, when compared to published baseline values for the same estuary. The demersal fish species C. spixii and G. genidens had the highest concentrations of As, Cr, Mn, Hg, and Se in both, hepatic and muscle, tissues. Trace metal bioaccumulation in fish was correlated with the biosynthesis of metallothionein and reduced glutathione in both, liver and muscle, tissues, suggesting active physiological responses to contamination sources. The trace metal concentrations determined in fish tissues were also present in the estuarine sediments at the time of this study. Some elements had concentrations above the maximum permissible limits for human consumption in fish muscles (e.g., As, Cr, Mn, Se and Zn), suggesting potential human health risks that require further studies. Our study supports the high biogeochemical mobility of toxic elements between sediments and the bottom-dwelling biota in estuarine ecosystems.

Keywords: Environmental pollution; Estuaries; Health risk assessment; Metalloproteins; Rio Doce.

Figure 1. Map of the sampling stations in the Rio Doce estuary, Brazil in August 2017.

Fundão dam failure area (star), sediment sampling (circles), and fish sampling areas (rectangle).

Figure 2. Total metallothionein and reduced glutathione concentrations (μmol g⁻¹ wet weight) in estuarine fishes liver and muscle tissues in the Rio Doce estuary.

Box plots indicate minimum, maximum, median, quartiles, and outliers (cicle). The asterisk indicates significance at p < 0.05.

Figure 3. Canonical analysis of principal coordinates (CAP) indicating differences in expression of antioxidant biomarkers and the contribution of elemental contamination in estuarine fishes.

Vectors are based on Spearman correlation values > 0.5 (p < 0.05) for elements and scores for protein concentration and species (mean score among sampled). The proportions of data explained by axis 1 and 2 are in parentheses.