Environmental disasters associated with mining activities are a global concern due to the risks of contamination (Bowker and Chambers, 2015; Garcia et al., 2017; Gil-Jiménez et al., 2017). As an example, tailings traditionally stored in dams offer a great risk to multiple ecosystems that may be located thousands of kilometers away from the mining operations (Magris et al., 2019). Tailing spills can significantly affect ecosystems downstream, impacting vast landscapes, rivers, cities, forests, crops, and lead to economic, social and ecological losses, in most cases with permanent effects (Bowker and Chambers, 2015).

In Brazil, the Samarco mine tailing disaster that occurred in November 2015 is an emblematic case of environmental disaster involving a dam failure, which caused significant impacts on terrestrial and aquatic systems (Gabriel et al., 2020a, 2020b; Gomes et al., 2017; Queiroz et al., 2018). Within days, the mine tailings spill silted up the watercourses downstream, buried houses, vegetation, and animals, and caused 19 human casualties (Carmo et al., 2017). In addition, the tailings traveled 600 km downriver and reached the Rio Doce estuary, permanently increasing sediment metal(loid) concentrations, burying, and killing benthic organisms and generating a tailing layer approximately 5 cm deep (Bernardino et al., 2019; Gomes et al., 2017; Queiroz et al., 2018).

The long-term effects of these impacts are yet largely unclear, even though there are multiple efforts in monitoring the aquatic ecosystems of the Rio Doce basin. In the Rio Doce estuary, the tailings arrived in association with toxic metals and metalloids (Queiroz et al., 2018; Sá et al., 2021), which increased the ecological risks to many aquatic species (Bernardino et al., 2019; Gabriel et al., 2020b). Moreover, biogeochemical processes in the estuary likely favor the long-term release of contaminants to the aquatic biota (Queiroz et al., 2018, 2021a), which suggests that this ecosystem will be a long-term hotspot for contaminants from the remaining tailings deposited over the Rio Doce upper basin, and a potential source of toxic compounds to the aquatic biota (Queiroz et al., 2018, 2021a, 2021b; Riba et al., 2002). These hypotheses have been partially supported by evidence showing that sediment metal concentrations (e.g., Al, Cr, Fe, and Mn) are not only associated to spatial changes in benthic assemblages within the estuary, but also that metals bound to Fe oxyhydroxides are being gradually released and bioaccumulating in fish, due to the reductive dissolution of Fe oxyhydroxides (Bernardino et al., 2019; Gabriel et al., 2020b; Queiroz et al., 2021a, 2021b).

In this sense, consolidating environmental quality indices from the Rio Doce estuary over multiple years is fundamental to assess the status of metal(loid)s pollution and its potential ecological risks (Liu et al., 2016). Sediment quality guidelines (SQGs) have been recognized as suitable tools to access the effects of toxic metals for both aquatic and human life. Methods of risk assessment can also assist in the proposal of measures for remediation, management strategies, and ecosystem monitoring. In fact, the integration and summarization of complex scientific data into single-values easily interpretable make these indices useful and applicable tools in communication with risk managers and decision-makers (Protano et al., 2014; Wilson and Jeffrey, 1994).

Several naturally occurring biogeochemical processes in estuarine sediments and soils can control the stability of metal-colloid interactions and, thus, the bioavailability of metals in estuarine ecosystems (Machado et al., 2016; Pejman et al., 2015; Segura et al., 2016; Wang and Chen, 2000). Hence, following the initial deposition of the Fe mine tailings in the Rio Doce estuary and their continued transport along the river basin, a long-term increase in metal(loid) concentrations in the estuary was registered (Queiroz et al., 2018, 2021a,b,c). Thus, there is a pressing need to understand the ecological risks in the Rio Doce estuary.

In this study, we monitored the Rio Doce estuarine sediments from August 2017 to January 2020 (1.9–4.2 years after the short-term impact) and pre-impact data were integrated from a previously published dataset (December 2015). Our objectives were to (1) determine the concentrations of the metal(loid)s (As, Cd, Co, Cr, Cu, Mn, Ni, Pb, and Zn) in the sediments along the Rio Doce estuary; (2) to explore the degree of metal(loid) contamination using contamination indices; (3) to assess environmental risks of these metal(loid)s by comparison with sediment quality guidelines (SQGs) and the potential ecological risk of metal(loid)s for the ecosystem; (4) to determine the main metal(loid)s that contribute to the ecological risk in the estuary.

The contamination of the Rio Doce estuarine sediments changed during the 4.2 years since the disaster in 2015, with an observed peak of sediment metal(loid) concentrations in 2017, followed by a period of stability until 2020. The higher metal(loid) concentrations in 2017 evidenced that nearly two years after the disaster, the estuary was being a significant sink of tailings and associated metals from the upper river basin (Gabriel et al., 2020a). As a consequence of the disaster, significant amounts of tailings were accumulated along the river basin and riparian ecosystems, and our data support that part of those tailings was being continually transported towards the estuary and bound to metals (Feng et al., 2011; Gabriel et al., 2020a; Queiroz et al., 2018). However, after the peak in 2017, the concentration of most metal(loid)s (except Pb) in the estuary decreased by an average 65.9%, with highest reductions in Cd (97.2%), Mn (73.5%), and Cr (70.5%). Our data then supports the continued transport of tailings and bound metals from the estuary to the Atlantic Ocean (Richard et al., 2020).

The decrease in metals concentrations may be associated with an increased grain size and a decrease in Fe content over time, which may suggest that there is a net transport of tailings outside the estuary, and biogeochemical transformation of tailings in estuarine soils. Based on satellite monitoring, there are multiple studies that suggest that the tailings are being continually transported to the coast after the disaster and potentially being accumulated on the inner shelf (Magris et al., 2019; Rudorff et al., 2018; Coimbra et al., 2019). Rudorff et al. (2018) reported an increase in coastal water turbidity after the disaster and suggested extensive plumes over the coastal zone that would be intensified during rainfall periods. We observed a temporal stability in estuarine contamination from 2018 to 2020 with limited evidence for a seasonal variability, which supports the hypothesis of a press disturbance over coastal ecosystems that are in short distances from the Rio Doce estuary (Magris et al., 2019). There has been so far limited evidence for the accumulation and ecological effects of tailings over the seafloor at distances of over 10 km from the Rio Doce mouth (Richard et al., 2020), even though tailings may be transported along with the river plume at greater distances.

The transport of tailings out of the estuary may be facilitated by the absence of bottom vegetation, which would help to capture the finer fractions (i.e., silt and clay; Sand-Jansen, 1998). As a result of strong bottom transport in the Rio Doce estuary, the lower contents of finer particles decrease the sediment binding capacity due to elevated sand and low organic matter content. It is important to highlight that the metal binding to sediments of the Rio Doce estuary occurs by adsorption and complexation processes, mainly in sediments with fine particles and/or with a high organic matter (Rainbow, 2007; Wang et al., 2015). Likewise, metal(loid) mobility and availability in the superficial sedimentary layer are associated with the sediment granulometry, salinity, organic matter content and Fe oxides from tailings (Machado et al., 2016; Queiroz et al., 2021c). Given that metal(loid) contamination is continually higher than baseline levels, the hypothesis of the arrival of more tailings that have been retained along the banks and channel of the Rio Doce through rainfall-runoff events is further supported (Rudorff et al., 2018).

Even with an overall temporal stability, the metal(loid)s concentrations in the estuarine sediment persisted above the pre-impact reference values reported by Gomes et al. (2017). Thus, considering that Fe oxides are a geochemical marker for the tailings that were deposited in the Rio Doce estuary and its significant correlation with other metal(loid)s, there is strong evidence that the deposited tailings are maintaining a chronic contamination of the estuary for over 4.2 years (Fig. 8, Supplemental data Table S4). According to Queiroz et al. (2018), the deposited tailings on the estuary are mostly composed of Fe oxyhydroxides with a high concentration of associated metals. In addition, this mineral fraction is susceptible to mineral dissolution under suboxic/anoxic conditions, commonly found in estuarine sediments and soils (Lovley and Phillips, 1986; Du Laing et al., 2009). As a result of the dissolution of Fe oxyhydroxides (i.e., dissimilatory Fe reduction), the associated metals are released increasing their bioavailability (Bonneville et al., 2004; Lambais et al., 2008; Queiroz et al., 2018, 2021a, 2021b, 2021c). This mechanism of dissimilatory Fe reduction poses a risk of contamination since it may expose aquatic organisms and probably cause lethal or sub-lethal biological effects (He et al., 2018; Worms et al., 2006).

Fig. 8.

Correlation between total Fe and metal(loid)s concentrations in bottom estuarine sedimentary samples from the Rio Doce estuary in 2015 (November; Gomes et al., 2017), 2017 (August), 2018 (January and August), 2019 (February), and 2020 (January).

(0.45MB).

The overall health of the Rio Doce estuary has declined significantly. The concentrations of metals that are now deposited in the Rio Doce estuary is comparable to other heavily polluted estuaries in Brazil, including urbanized estuaries in the region (Hadlich et al., 2018). The high concentration of metal(loids) in sediments impacts benthic assemblages as several species may be intolerant to their toxicity (Bernardino et al., 2019). Benthic assemblages are a critical component of estuarine food webs and may transfer contaminants to higher trophic levels through bioaccumulation and biomagnification processes, for instance, humans (Gabriel et al., 2020b; Jędruch et al., 2019; Tarras-Wahlberg et al., 2001). As a result, the sediments from the Rio Doce estuary may be considered polluted and chronic effects on sedimentary organisms are expected since Cd and Pb values exceed the PEL level and As, Cr, Cu, and Ni of the TEL level according to Canadian sediment quality guidelines (Table 2). However, such comparative method with guideline values for temperate environments may underestimate the assessment by not considering the local natural geochemical background, and complementary ecotoxicological assessments are necessary to assess possible metal toxicities for the environment.

In this sense, ecological risk indices (CFi, Pi, and RI) (Figs. 3, 4 and 6), and effects-based sediment quality guidelines (SQG) can support the hypothesis of long-term sediment contamination of the Rio Doce estuary since the impact in 2015. The Cd, Cr, Mn, and Zn in 2017 (August) and 2018 (January and August) induced a general increase in ecological risk exceeding the very high ecological risk limit (RI ≥ 600; Fig. 7). Our data support that estuarine sediments may cause adverse effects on aquatic life and human health, even 4.2 years after the disaster. Our results also support the possibility of contamination of the biota by metal(loid)s such as As, Cr, Cu, Mn, and Zn. The effects of metal bioaccumulation and oxidative stress in fish have been detected in the Rio Doce estuary and in contaminated areas upstream (Ferreira et al., 2020; Gabriel et al., 2020b; Weber et al., 2020). Current high levels of Cr, Cu, Mn, and Zn may lead to toxic effects in other organisms (Li et al., 2013). On another hand, episodic peaks in sediment Pb are also of concern as the observed concentrations were significantly above the reference values for the Rio Doce estuary (Gomes et al., 2017). These peaks differ from the overall pattern of other metal(loid)s studied and may be related to other human-related sources, likely from a combination of heavily industrial and agricultural uses of the Rio Doce upper basin. It is also important to note that all forms of Pb are extremely toxic to humans as well as most other living organisms (Sayadi et al., 2010; WHO, 2019). In addition, there is no level of exposure to lead that is known to be unharmful, since, even at low concentrations, it can pose a greater threat to aquatic life compared to other metals (Bastami et al., 2014; WHO, 2019).

Toxic effects in aquatic environments may cause serious consequences to human health, especially when coastal communities depend on fish protein for their subsistence (Bashir et al., 2020; Zhou et al., 2008). Bioaccumulation effects of tailing-associated metals in the Rio Doce have been detected in bottom dwelling fish (Gabriel et al., 2020b; Queiroz et al., 2021a), which allied to a continued ecological risk assessment of the estuary and supports the maintenance of the prohibition of fishing activities. There is urgent need to access and quantify other potential sources of contaminants to local populations near the Rio Doce estuary, as these will be key for determining long-term health risks.

Besides the risks for the aquatic life and human health, the Fundão dam failure can be considered the largest dam disaster in terms of the volume of spilled tailings, the size of the affected area, and the extent of socio-environmental impacts, when compared to other major environmental disasters involving mining dams (Table 3). The large proportion of the disaster and the ineffective strategies to retain the mine tailings spilled in aquatic environments led to severe environmental impacts and likely infeasible clean-up strategies (Carmo et al., 2017). Therefore, without an effective initial action to remove the deposited tailings, terrestrial, riverine and coastal ecosystems will be continually under the effects of tailings (Carmo et al., 2017; Gabriel et al., 2020a,b). The consequence of the lack of short-term actions brought ecological implications to the aquatic environments from the molecular to the community level, having a direct impact on ecosystem services and, therefore, on the subsistence and food security of the affected regions (Gabriel et al., 2020b; Gomes et al., 2017; Quadra et al., 2019; Weber et al., 2020). This experience shows that efforts should be placed on prevention rather than reacting after the event. Therefore, the Rio Doce disaster has raised global concern and alarm about the pollution of natural environments caused by mining and dam failures.

Effective decontamination action plans and restoration of ecological integrity are crucial to improving the long-term environmental status of affected aquatic environments. Some experimental initiatives using different soil amendments seem promising in removing metal(loid)s from inundated soils on the estuary (Ferreira et al., 2021). It is clear that further research into recovery processes is urgently needed and will be crucial for food and water security of impacted communities, and protection of the biodiversity. In addition, recovery actions would help to protect the ecosystem services that the local region provide (Brito et al., 2021). Although plans for short, medium, and long-term recovery actions for the Rio Doce basin were determined by a Term of Transaction and Conduct Adjustment (TTAC) signed by Samarco (Vale and BHP), the Brazilian federal and state governments, recovery actions on the estuarine part of the basin were never put in place. According to the document that defines the repair actions, the Renova foundation is responsible for executing recovery actions, including the implementation of tailings containment systems and in situ treatment of rivers impacted (see Fundação Renova, 2021).

Our results show the persistence of potentially toxic elements in the Rio Doce estuary, and restoration actions need to consider environmental and human health improvements (Couto and Brandespim, 2020; WHO, 2016; Zhou et al., 2008). These actions will need to be aligned with the Integrated Water Resources Plan (PIRH) prepared for the Rio Doce basin, which has as one of the objectives the promotion of a water quality for human health, aquatic life, and environmental quality (see CBH-Doce, 2016). However, the plan actions and investments involve the creation of additional protected areas and basic sanitation, but these will be largely ineffective to cease the effects of tailings in the estuarine biota. We envision no recovery for the estuarine health unless strategies that promote a removal of tailings and their associated metal(loids) in soils are implemented.

In summary, the Rio Doce estuary continues to be heavily impacted by the tailings and the associated contaminants nearly 5 years after the short-term impacts, with significant ecological and human health risks. Management measures have never been put in place on this particular region, but the source-to-sea system and the landscape approach can be the entry point for implementing restoration programs (Brito et al., 2021). The source-to-sea system offers an alternative to integrate the different issues that affect the quality of the watershed, as well as its adjacent coastal and marine areas; while the landscape approach seeks to integrate policies and practices for multiple land uses through the implementation of adaptive and integrated management (Brito et al., 2021; Mathews et al., 2019). Given the long path of the tailings to reach the Atlantic Ocean and the socio-environmental impacts associated, it will be necessary to deal with land and sea together to face the long-term consequences of the disaster, offering a better basis for environmental management and governance.

Our findings reveal that the Rio Doce estuary is working as a sink of tailings from the Samarco disaster for nearly 5 years, and will likely be a source of contaminants to the biota for decades to come. Despite a temporal stability in metal(loid)s concentrations from 2018 to 2020, the levels still remain well above the baseline reference values for the estuary and often reach sediment quality thresholds. Therefore, the potential health risks to the environment, biota, and consequently, to local communities remain at unacceptable levels and effective actions for decontamination of the Rio Doce estuary are a priority. Fe-rich tailings will likely bind and release metal(loid)s for a long period of time within the estuary and will offer great risk to humans through consumption of contaminated fish. For that reason, our results support the maintenance of the fishing bans, the need to monitor public health near the estuarine region, as well as implementation of recovery and decontamination actions along with integrated coastal and freshwater management.

This work was funded by the Fundação de Amparo à Pesquisa e Inovação do Espírito Santo (FAPES), Conselho Nacional de Pesquisa e Desenvolvimento (CNPq) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) grant Soil Benthos Rio Doce Network Project to AFB and TOF (FAPES 77683544/17). FAPES grant to FÂG; FAPESP grant to ADF (2019/14800-5) and HMQ (2018/04259-2); CAPES/PRINT grant to ALSV (88887.370137/2019-00). AFB and TOF were also supported by CNPq PQ grants (grants number 301191/2017-8 and 305996/2018-5, respectively).

The authors declare that there is no conflict of interest regarding the publication of this article.