Assessment of oxidative stress and bioaccumulation of the metals Cu, Fe, Zn, Pb, Cd in the polychaete Perinereis gualpensis from estuaries of central Chile

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Abstract

The estuaries of the Aconcagua and Maipo Rivers of central Chile are receptors of residues that contain metals from anthropic activities including agriculture, mining and smelters, which have different levels in the two basins. This study postulates that the exposition to metals is different in the two estuaries and that their sediments contain bioavailable chemical agents that produce oxidative stress. The aim of the study was to evaluate the effect of estuarine sediments on the polychaete Perinereis gualpensis using oxidative stress biomarkers and to determine the metal concentrations in sediments and their accumulation in P. gualpensis. Sediments and organisms were collected in December 2015 and January 2016 in the estuaries. The Catapilco estuary was used as control, since its basin has little anthropic activity. The metal concentrations of Fe Cu, Pb, Zn and Cd were determined in tissues of the organisms and in sediments. The granulometry, conductivity, redox potential, pH and organic matter in sediments were determined, as well as catalase activity and lipid peroxidation. The results show that the concentrations of metals in sediments were higher in the estuary of the Aconcagua River: Cu: 48 ± 2 μg g−1; Fe: 154 ± 19 mg g−1, Pb: 20 ± 3 μg g−1 and Zn: 143 ± 20 μg g−1. In tissues, Pb and Fe were higher in the estuary of the Maipo River, while Cd was detected only in the Catapilco River mouth. Catalase activity was greater in the estuary of the Aconcagua River and lipid peroxidation in the estuary of the Catapilco River. Significant regressions were found between biomarkers of oxidative stress and metal concentrations in tissues of P. gualpensis. In conclusion, the sediments of the studied estuaries contain bioavailable chemical agents that provoke oxidative stress in P. gualpensis, which may be a risk for the benthic communities of these ecosystems. This species is proposed to monitor metals bioavailability and oxidative stress in estuarine sediments.

Introduction

Estuarine systems integrate marine, coastal and fluvial systems through water flow, sediment and dissolved substances, constituting a socio-ecological system. Although it is an ecosystem itself, it cannot act alone since it largely depends on other ecosystems. In addition to the processes and ecological functions, the cumulative effects of human activity should be included both upstream and downstream (Pallero et al., 2017)

Estuaries represent ecosystems of high productivity and are crucial in the life histories of many fish, invertebrates, birds, etc. (Monserrat et al., 2007, Díaz-Jaramillo et al., 2010). The sustainability of these water bodies is vital for coastal regions in ecological and economic terms. However, estuaries are potentially exposed to chemical contaminants transported by rivers from urban and industrial areas, because they are sediment deposition areas. Estuaries have become the principal reservoir for a large number of chemical substances introduced into the aquatic ecosystem by human activity (Thompson de Oliveira Lemos et al., 2014). Complex mixtures of contaminants can enter the aquatic environment via effluents or surface runoff, and thus aquatic organisms can be inevitably exposed (Blanchet- Letrouvé et al., 2013).

The deterioration of estuaries due to the presence of metals and organometals results mainly from anthropic activities. Due to their tendency to accumulate in aquatic organisms, these contaminants compromise the water quality and the health of biotic estuarine communities (Tapia et al., 2009, Tapia et al., 2012). Metals tend to bind covalently with macromolecules such as proteins and DNA. This binding causes oxidative stress (Srivastava et al., 2006, Fevzi et al., 2007). The transition metals, among other sources, change the metabolism of organisms by stimulating reactive oxygen species (ROS) production by the Fenton and Haber–Weiss reactions (Monserrat et al., 2007, Jara et al., 2014).

Organisms respond to chemical agents through the antioxidant systems located in subcellular organelles, providing protection. They have been traditionally called non-enzymatic defenses and enzymatic defenses. The former do not interact directly with free radicals generated from O2 (O−2) or the product of dismutation, while the latter have to do with the repair or removal of damaged biological structures (Pal Yu, 1994; Monserrat et al., 2007). The enzymes known as Phase I (solubilization) and Phase II (conjugation) of xenobiotic metabolism are essential in the process of detoxification, involving on one hand ROS and on the other hand free radical-metabolizing enzymes (e.g. superoxide dismutase, catalase, glutathione peroxidase, glutathione-S-transferases). These enzymes are good biomarkers for determining biological effects of exposure to pollutants (Díaz-Jaramillo et al., 2013).

Metals tend to accumulate in aquatic ecosystem sediments, depending on factors such as grain size, organic matter and redox potential (Gray and Elliott, 2009). Therefore, organisms inhabiting these sediments (benthic assemblages) may be exposed to metals and exhibit toxic effects (Campana et al., 2012; Fossi et al., 2012). These organisms are key to the food web of estuarine ecosystems. They include polychaetes, which are commonly used in eco-toxicological bioassays (Díaz and Reish, 2009) as indicators of bioaccumulation of chemical agents, the health status of subtidal sediments and contamination by the analysis of community variables (Cañete et al., 2000, Giangrande et al., 2005, Dean, 2008).

The effect of contamination on organisms that live in the sediments in Chile has been determined through changes in the structure of communities such as diversity, species richness, and abundance (Bertrán et al., 2001a). These ecological methods are time-consuming and expensive. Chemical analytical methods may detect and determine concentrations of the chemical agents, but these do not provide direct information on potentially adverse effects. Therefore, there is currently growing interest in using molecular biomarkers to determine the oxidative damage produced by metals in organisms which inhabit aquatic environments, as a useful tool to provide early warning (Carvalho-Neta and Abreu-Silva, 2010, Jara et al., 2014)

The nereidid polychaete Perinereis gualpesis is very abundant in estuaries of southern Chile, with densities greater than 2000 ind/m2 (Jaramillo et al., 2001). Preliminary studies have shown that this species is an efficient biomonitor for heavy metals in these environments (Bertrán et al., 2001b, Díaz-Jaramillo et al., 2017). The sub-organism response level in this species has been proposed as a biomarker and it could be a potential tool to determine the state of environments experiencing numerous types of anthropogenic stressors.

The estuaries of the Aconcagua and Maipo Rivers of central Chile are considered category one priority sites for biodiversity conservation in the Valparaíso Region (CONAMA, 2005). However, important anthropogenic activities such as mining, industry and agriculture take place in their basins. These activities generate wastes containing metals such as copper, zinc, iron, manganese, arsenic and lead, among others, which can reach these aquatic ecosystems and accumulate in the estuarine sediments. Since the basins of these rivers have different levels of human activity, it is likely that there are different levels of exposure in the sediments of their estuaries. There is currently no information about the levels of exposition of benthic organisms in these estuaries. This information is fundamental to determine the environmental risk due to metals in these estuary zones. This study postulated that the estuarine sediments of these rivers contain concentrations of bioavailable chemical agents that cause oxidative damage and antioxidant response in the macrozoobenthos organisms. Thus the aim of this study was to evaluate the effect of estuarine sediments on the polychaete Perinereis gualpensis using oxidative stress biomarkers and to determine the metal concentrations in sediments and the bio-accumulation in P. gualpensis.

Section snippets

Study area

The Maipo River basin covers an area of 15,304 km2. The basin covers almost 100% of the Metropolitan Region and a minimal area of the Regions of Valparaiso (San Antonio and Valparaiso Provinces) and Libertador Bernardo O′Higgins (Cachapoal Province). The total population in the basin is 4668,473. The average annual flow is 99 m3/s. The Aconcagua River basin covers an area of 7200 km2 with a total population of 1000,000 people. It is located in the southern end of the area of the transverse or

Sampling

Sampling was performed in December 2015 and January 2016. The sampling points were: Aconcagua River estuary, 32°55′3.66″ S, 71°30′28.26″ W; Maipo River estuary, 33°37′8.57″S, 71°37′45.40″W and Catapilco River estuary, 35°37′53.74″S, 71°25′44.89″W. The organisms were separated and collected from the sediments manually using a 500 µ sieve. Four replicates were taken at each site. The collected sediments were transported to the laboratory in plastic containers and frozen at −20 °C. The organisms

Physical and chemical parameters of sediments in the estuaries

The pH of sediments tended to alkalinity, while there were similar percentages of organic matter among estuaries (Table 1). These results suggest that although the basins have different levels of human impact, they have the same self-purification or assimilative capacity. The pH and organic matter were similar to the values reported by Díaz-Jaramillo et al. (2013) in the Lenga and Raqui estuaries. However, the organic matter was lower in our study compared to the Tornagaleones and Valdivia

Conflict of interest

The authors declare that they have no conflicts of interest.

Acknowledgments

This study was financed by the Centro de Investigación y Gestión de Recursos Naturales (CIGREN) of Universidad de Valparaíso (DIUV/2003).

References (45)

  • S. Zhao

    Salinity increases the mobility of Cd, Cu, Mn, and Pb in the sediments of Yangtze Estuary: relative role of sediments' properties and metal speciation

    Chemosphere

    (2013)
  • ATSDR

    Toxicological Profile for Copper

    (1990)
  • C. Bertrán et al.

    Macrofauna del curso inferior y estuario del río Biobío (Chile): cambios asociados a variabilidad estacional del caudal hídrico

    Rev. Chil. Hist. Nat.

    (2001)
  • C. Bertrán

    Perinereis gualpensis Jeldes (Annelide, Polychaeta) como biomonitor de metales pesados en la desembocadura del rio Biobio (Chile)

    Inform. Tecnológica

    (2001)
  • S.J. Blott et al.

    Gradistat: a grain size distribution and statistics package the analysis of unconsolidated sediments

    Earth Surf. Process Landf.

    (2001)
  • O. Campana

    Sub-lethal effects of copper to benthic Invertebrates explained by sediment properties and dietary exposure

    Environ. Sc. Technol.

    (2012)
  • R. Carvalho-Neta et al.

    Sciades herzbergii oxidative stress biomarkers: an in situ study of an estuarine ecosystem (São Marcos' Bay, Maranhão, Brazil)

    Braz. J. Oceanogr.

    (2010)
  • I. Cañete et al.

    Proposición de un índice de vigilancia ambiental basado en la variabilidad temporal de la abundancia de dos especies de poliquetos bentónicos de bahía Quintero, Chile

    Rev. De. Biol. Mar. Y. Oceanogr.

    (2000)
  • J. Cataldo

    Use of molecular biomarkers in Eisenia foetida to assess copper toxicity in agricultural soils affected by mining activities

    J. Soil Sci. Plant Nutr.

    (2011)
  • CONAMA

    Estrategia y Plan de Acción Para la Conservación de la Diversidad Biológica

    (2005)
  • H.K. Dean

    The use of polychaetes (Annelida) as indicator species of marine pollution: a review

    Rev. De. Biol. Trop.

    (2008)
  • Díaz-Jaramillo

    Sublethal effects in Perinereis gualpensis (Polychaeta: nereididae) exposed to mercury-pyrene sediment mixture observed in a multipolluted estuary

    Ecotoxicology

    (2017)
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