Long-term impacts on estuarine benthic assemblages (2015-2020) after a mine tailing spill in SE Brazil.

The Rio Doce estuary was critically impacted in 2015 by the world's largest mining tailing spill, with still unclear long-term effects on the aquatic biota. Here we present a long-term (2015 to 2020) assessment of estuarine benthic assemblages, where we demonstrate that despite a decline in the absolute concentrations of potentially toxic elements; sediment contamination is still above pre-impact conditions. The presence of these contaminants is likely responsible for a continued low habitat quality for the benthic fauna, characterized by a reduction of 96 % of the macroinvertebrate density and persistent change in the benthic assemblage composition. Our study supports previous work indicating the long-term nature of pollution impacts in estuaries, and demonstrate that although water quality levels were quickly adequate under regulatory terms, they largely lack significance to the overall ecosystem health assessment, as they are not related to the recovery of bottom- dwelling assemblages in estuarine ecosystems.

Benthic bioturbation: A canary in the mine for the retention and release of metals from estuarine sediments.

After the largest mining tailings spill in Brazil, the Rio Doce estuarine ecosystem was severely impacted by metal contamination. In a 28-day laboratory experiment, we examined the effects of the polychaeta Laeonereis sp. on fluxes of oxygen and metal across the sediment-water interface. The density-dependent effect of Laeonereis sp. in the oxygen and metal fluxes was tested at low and high (74 and 222 ind m-2, respectively) densities, and compared with defaunated controls. The higher worm density had an amplified effect on the oxygen flux, sediment uptake of Al and Mn, and Fe oxidation compared with the control, but no significant effects on other metals (Ba, Cd, Co, Cr, Cu, Ni, and Zn). Higher worm density increased the oxidation of Fe phases, but no effect in the solid phase of other metals. Consequently, Laeonereis sp. bioturbation prevents the reduction of Fe phases and the release of metal-bound-contaminants to estuarine systems.

Manganese: The overlooked contaminant in the world largest mine tailings dam collapse.

Manganese (Mn) is an abundant element in terrestrial and coastal ecosystems and an essential micronutrient in the metabolic processes of plants and animals. Mn is generally not considered a potentially toxic element due to its low content in both soil and water. However, in coastal ecosystems, the Mn dynamic (commonly associated with the Fe cycle) is mostly controlled by redox processes. Here, we assessed the potential contamination of the Rio Doce estuary (SE Brazil) by Mn after the world's largest mine tailings dam collapse, potentially resulting in chronic exposure to local wildlife and humans. Estuarine soils, water, and fish were collected and analyzed seven days after the arrival of the tailings in 2015 and again two years after the dam collapse in 2017. Using a suite of solid-phase analyses including X-ray absorption spectroscopy and sequential extractions, our results indicated that a large quantity of MnII arrived in the estuary in 2015 bound to Fe oxyhydroxides. Over time, dissolved Mn and Fe were released from soils when FeIII oxyhydroxides underwent reductive dissolution. Due to seasonal redox oscillations, both Fe and Mn were then re-oxidized to FeIII, MnIII, and MnIV and re-precipitated as poorly crystalline Fe oxyhydroxides and poorly crystalline Mn oxides. In 2017, redox conditions (Eh: -47 ± 83 mV; pH: 6.7 ± 0.5) favorable to both Fe and Mn reduction led to an increase (~880%) of dissolved Mn (average for 2015: 66 ± 130 µg L-1; 2017: 582 ± 626 µg L-1) in water and a decrease (~75%, 2015: 547 ± 498 mg kg-1; 2017: 135 ± 80 mg kg-1) in the total Mn content in soils. The crystalline Fe oxyhydroxides content significantly decreased while the fraction of poorly ordered Fe oxides increased in the soils limiting the role of Fe in Mn retention. The high concentration of dissolved Mn found within the estuary two years after the arrival of mine tailings indicates a possible chronic contamination scenario, which is supported by the high levels of Mn in two species of fish living in the estuary. Our work suggests a high risk to estuarine biota and human health due to the rapid Fe and Mn biogeochemical dynamic within the impacted estuary.

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

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.

Ecological Risks of Metal and Metalloid Contamination in the Rio Doce Estuary.

The rupture of a mining dam in southeastern Brazil in 2015 was the country's greatest environmental tragedy. In order to evaluate the ecological risks of the mine tailings on the Rio Doce estuary, this study assessed trace metal contamination and sediment quality indices up to 2.9 y after the dam rupture. Surface sediments were collected from 17 stations on the Rio Doce estuary and Cd, Pb, Cr, Zn, Cu, and As concentrations were determined by inductively coupled plasma atomic emission spectroscopy (ICP-OES). Four ecological risk indices (modified contamination degree [mCd], pollution load index [PLI], risk index [RI], and sediment quality guideline quotient [SQG-Q]) suggest a high risk by metal contamination with possible adverse biological effects, with moderate seasonal variability. Based on a precautionary approach, our results support fisheries closures and the need for public health monitoring in the affected areas, and support other studies that suggest chronic metal contamination of the Rio Doce estuary. Integr Environ Assess Manag 2020;16:655-660. © 2020 SETAC.

A ruptura de uma barragem de mineração no sudeste do Brasil em 2015 causou a maior tragédia ambiental do país. Para avaliar os riscos ecológicos dos rejeitos de minério no estuário do Rio Doce, este estudo avaliou os índices de contaminação por metais traços e qualidade dos sedimentos até 2,9 anos após a ruptura da barragem. Os sedimentos de superfície foram coletados em 17 estações no estuário do Rio Doce e as concentrações de Cd, Pb, Cr, Zn, Cu e As foram determinadas por ICP-OES. Quatro índices de risco ecológico (mCd, PLI, RI e SQG-Q) sugerem um alto risco de contaminação por metais com possíveis efeitos biológicos adversos, com variabilidade sazonal moderada. Com base em uma abordagem preventiva, nossos resultados apoiam o fechamento da pesca e a necessidade de monitoramento da saúde pública nas áreas afetadas, além de apoiar outros estudos que sugerem contaminação crônica por metais no estuário do Rio Doce. Integr Environ Assess Manag 2020;16:655-660.

Chronic trace metals effects of mine tailings on estuarine assemblages revealed by environmental DNA.

Mine tailing disasters have occurred worldwide and contemporary release of tailings of large proportions raise concerns of the chronic impacts that trace metals may have on the aquatic biodiversity. Environmental metabarcoding (eDNA) offers an as yet poorly explored opportunity for biological monitoring of impacted aquatic ecosystems from mine tailings and contaminated sediments. eDNA has been increasingly recognized to be an effective method to detect previously unrecognized small-sized Metazoan taxa, but their ecological responses to environmental pollution has not been assessed by metabarcoding. Here, we evaluated chronic effects of trace metal contamination from sediment eDNA of the Rio Doce estuary, 1.7 years after the Samarco mine tailing disaster, which released over 40 million m3 of iron tailings in the Rio Doce river basin. We identified 123 new sequence variants environmental taxonomic units (eOTUs) of benthic taxa and an assemblage composition dominated by Nematoda, Crustacea and Platyhelminthes; typical of other estuarine ecosystems. We detected environmental filtering on the meiofaunal assemblages and multivariate analysis revealed strong influence of Fe contamination, supporting chronic impacts from mine tailing deposition in the estuary. This was in contrast to environmental filtering of meiofaunal assemblages of non-polluted estuaries. Here, we suggest that the eDNA metabarcoding technique provides an opportunity to fill up biodiversity gaps in coastal marine ecology and may become a valid method for long term monitoring studies in mine tailing disasters and estuarine ecosystems with high trace metals content.