Pulmonary oxidative stress in wild bats exposed to coal dust: A model to evaluate the impact of coal mining on health

https://doi.org/10.1016/j.ecoenv.2020.110211Get rights and content

Highlights

  • The levels of several chemical elements were higher in bats from coal mining areas.

  • Bats inhabiting coal mining areas showed increase in pulmonary emphysema degree.

  • ROS and DCF levels increased in the lung of bats from coal mining areas.

  • CAT activity, Nitrite and GSH levels decreased in the lung of bats from coal areas.

  • Bats could be act as sentinel species of harmful effects of coal to human health.

Abstract

This study aimed to verify possible alterations involving histological and oxidative stress parameters in the lungs of wild bats in the Carboniferous Basin of Santa Catarina (CBSC) state, Southern Brazil, as a means to evaluate the impact of coal dust on the health of wildlife. Specimens of frugivorous bat species Artibeus lituratus and Sturnira lilium were collected from an area free of coal dust contamination and from coal mining areas. Chemical composition, histological parameters, synthesis of oxidants and antioxidant enzymes, and oxidative damage in the lungs of bats were analyzed. Levels of Na, Cl, Cu, and Br were higher in both species collected in the CBSC than in the controls. Levels of K and Rb were higher in A. lituratus, and levels of Si, Ca, and Fe were higher in S. lilium collected in the carboniferous basin. Both bat species inhabiting the CBSC areas exhibited an increase in the degree of pulmonary emphysema compared to their counterparts collected from control areas. Sturnira lilium showed increased reactive oxygen species (ROS) and 2′,7′-dichlorofluorescein (DCF) levels, while A. lituratus showed a significant decrease in nitrite levels in the CBSC samples. Superoxide dismutase (SOD) activity did not change significantly; however, the activity of catalase (CAT) and levels of glutathione (GSH) decreased in the A. lituratus group from CBSC compared to those in the controls. There were no differences in NAD(P)H quinone dehydrogenase 1 protein (NQO1) abundance or nitrotyrosine expression among the different groups of bats. Total thiol levels showed a significant reduction in A. lituratus from CBSC, while the amount of malondialdehyde (MDA) was higher in both A. lituratus and S. lilium groups from coal mining areas. Our results suggested that bats, especially A. lituratus, living in the CBSC could be used as sentinel species for harmful effects of coal dust on the lungs.

Introduction

Coal is a combustible, sedimentary rock constituted by organic elements, minerals, heavy metals, and other inorganic compounds (Chen et al., 2005; Dalal et al., 1995; León-Mejía et al., 2011), and fossilized over millions of years, similar to all fossil fuels (Castranova and Vallyathan, 2000; Gupta, 2007), which vary depending on the site of their origin (Donbak et al., 2005; Dontala et al., 2015). Despite the serious environmental impacts of mining and coal use (Adibee et al., 2013; Choi, 2015; Limbri et al., 2013; Sun et al., 2011; Zocche et al., 2014, 2017), coal is still an important resource used for electric power generation, once fulfilling 41% of global electricity needs (Bian et al., 2010; Dai and Finkelman, 2018; Yu, 2017).

Coal dust is a fine, powdered form of coal classified as a very dangerous fossil pollutant (León et al., 2007; Zakrzewski, 1991). It contains more than 50 chemical elements (Ketris and Yudovich, 2009), including heavy metals, and comprise inorganic compounds, like oxides, silica, and ash (Caballero-Gallardo and Olivero-Verbel, 2016; Finkelman, 1994; León et al., 2007; Singh et al., 2012, 2015). Nowadays, many coal mining sites are no longer active; however, the closure of mining areas does not mean the end of the polluting process, nor exhaustion of the source of pollution, because the environmental effects of coal mining persist for a long time (Dontala et al., 2015; Zocche et al., 2010).

Coal mining releases large amounts of coal dust (Huertas et al., 2012; Sinitsky et al., 2016; Yu, 2017) that is rich in chemical elements such as Co, Cu, Ni, Pb, Zn, Al, Cr, Mn, Co (Zocche et al., 2014, 2017), mineral nanoparticles, and inorganic substances (León-Mejía et al., 2014) that form heterogeneous compounds containing COX, NOX, SOX, Al, Si, crystals, quartz, and sulfur (León et al., 2007; Stephens and Ahern, 2001; Zhou et al., 2005). Once in the environment, these pollutants present a high risk to the health of wildlife, due to the potential synergistic effects of these complex mixtures (Dontala et al., 2015; Gold and Ames, 1990; Stephens and Ahern, 2001).

In addition, inhalation of dust generated during the extraction and deposition of coal can lead to significant harmful effects, especially those that affect the respiratory system, that can lead to morbidity and decreased life expectancy (Pinho et al., 2004). Workers in the coal industry, and wildlife and people who live near coal mining areas, are commonly exposed to coal dust and its contaminants, including heavy metals and quinones (Li et al., 2008) that can cause severe occupational hazards. The lungs are the first target sites of oxidants produced during oxygen combustion (Mossman, 2003).

Studies have suggested that, after exposure to industrial particles, significant biochemical changes occur in the lungs. Specifically, mineral coal, in addition to the toxic elements present in its composition, releases other components aggregated during extraction, such as silica and iron. These substances, after inhalation, can alter both the physical structure and the physiology of the pulmonary system (Tao et al., 2003). The activation of macrophages and recruitment of polymorphonuclear cells, caused by the deposition of industrial particles, probably results in the induction of lung damage. This process activates cytokines, chemokines, and ROS as inflammatory mediators, which promote local and systemic oxidative stress and, consequently, cause deleterious effects involving lung tissue (Mossman, 2003).

DNA damage from oxidative stress has been observed in peripheral blood lymphocytes of coal mining employees (Schins et al., 1995; Schoket et al., 1999). These effects arise from interaction between ROS and DNA, forming adducts with purines after metabolic activation (Baird et al., 2005; León-Mejía et al., 2011; Sinitsky et al., 2016). Additionally, other natural sources, such as ionizing radiation, also induce DNA damage through double-strand DNA breaks in coal miners (Robertson et al., 2013).

Biomonitors, also known as sentinel organisms, have been used for a long period to alert people about dangerous environments. For the selection of a biomonitor, the main aspects to be observed are: (a) the animals must share the same environment with humans; (b) respond in a similar fashion to toxic chemicals; and (c) develop similar pathologies in response to these effects (Silva et al., 2003). According to Jones et al. (2009), bats can serve as biomonitors for human health in mining areas, as well in other anthropic environments (Benvindo-Souza et al., 2019a, 2019b), since these animals are at the same trophic level and may accumulate toxic elements in their organs (O'Shea et al., 2001). Therefore, the objective of this study was to verify possible alterations in histological and oxidative stress parameters in the lungs of wild bats in the Carboniferous Basin of Santa Catarina state, Southern Brazil, as a model system to evaluate the impact of coal dust on the health of wildlife.

Section snippets

Description of the study areas

The study was carried out in two regions of south of Brazil, where one was free of contamination by coal mining activities (control area) and the other under the influence of coal mining activities (mined area). Bats were collected from the Natural Reserve of Salto Morato (25°10′ S and 48°15′W), a municipality of Guaraqueçaba, north of Parana state (control area), and from the municipalities of Criciúma (28°40′ S and 49°22′ W) and Treviso (28°30′ S and 49°27′ W), south Santa Catarina state, in

Chemical analysis of the lungs of bats

Table 1 presents the pulmonary levels of chemical elements on a dry weight (μg·g−1) basis, which varied across both the species and studied areas. The lung levels of Na, Cl, Cu, and Br in the individuals of both species from the coal mining areas were higher than those in animals collected from the control area. On the other hand, the lung levels of K and Rb in A. lituratus from coal mining areas were higher than in A. lituratus from the control area, while Si, Ca and Fe were higher in S. lilium

Discussion

Unlike organic substances, several chemical elements such as trace metals and metalloids are non-biodegradable and therefore remain in the soil and sediment compartments for a long time (Kabata-Pendias, 2011). This enduring permanence presents deleterious risks to human and wildlife health (Kabata-Pendias, 2011; Khan et al., 2010). In biochemical processes, chemical elements are recognized as being essential and non-essential, based on their physiological function (Kabata-Pendias, 2011).

Conclusions

The results of this study suggest that chronic exposure of bats to an environment filled with coal dust particles promotes histological and oxidative damage and, therefore, these animals may act as bioindicators of the ecotoxicological potential for wild populations that inhabit such coal dust particle-enriched areas. Additional studies are needed so that we can more accurately assess the damage generated in the respiratory and other organic systems of Chiroptera, and thus use these animals as

CRediT authorship contribution statement

Giulia dos Santos Pedroso-Fidelis: Investigation, Data curation, Writing - original draft. Hémelin Resende Farias: Investigation. Gustavo Antunes Mastella: Investigation. Liana Appel Boufleur-Niekraszewicz: Investigation, Data curation. Johnny Ferraz Dias: Investigation, Resources. Marcio Correa Alves: Investigation. Paulo Cesar Lock Silveira: Investigation, Formal analysis, Writing - original draft. Renata Tiscoski Nesi: Investigation, Formal analysis. Fernando Carvalho: Investigation,

Declaration of competing interest

The authors declare that there are no conflicts of interest.

Acknowledgments

The authors wish to thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil, and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil, for research support.

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