Occurrence of microplastics and heavy metals accumulation in native oysters Crassostrea Gasar in the Paranaguá estuarine system, Brazil

https://doi.org/10.1016/j.marpolbul.2021.112225Get rights and content

Highlights

  • Oysters were confirmed as effective bioindicators of environmental quality.

  • Particular attention with arsenic levels.

  • MPs were found at all sampled locations.

  • Influence of MPs on metals should be better studied.

Abstract

The ubiquitous presence of contaminants in the marine environment is considered a global threat to marine organisms. Heavy metals and microplastics are two distinct classes of pollutants but there are interactions between these two stressors that are still poorly understood. We examined the potential relationship between heavy metals (Al, Cr, Mn, Fe, Ni, Cu, Zn, As, Cd, Ba, Hg, Pb) and microplastic particles in oysters sampled along the Paranaguá Estuarine System. The results suggested high levels of As and Zn in the bivalves, which are destined for human consumption. Microplastic particles were found in oysters from all sampled locations, demonstrating the spread of this pollutant in the marine environment and its ability to bioaccumulate in oysters. However, our data did not demonstrate a direct relationship between microplastics and heavy metals, suggesting that these particles are not the main route for heavy metal contamination of oysters in the Paranaguá Estuarine System.

Introduction

Estuaries are important ecosystems that provide food and habitat for a large number of aquatic organisms, in addition to promoting biogeochemical processes for other environments through their connection between watersheds and coastal waters (Barletta et al., 2010; Costa and Barletta, 2016). However, there is an increasing anthropogenic interference in these environments, often caused by activities such as agriculture, industrial development and multiple uses of water, leading to inadequate waste disposal, sewage discharges and flow control (Barletta et al., 2019). Estuarine environments are thus considered important pools of heavy metals and other contaminants (Ip et al., 2004) and have attracted much attention from researchers (Hu et al., 2013; Venkatramanan et al., 2015; Wang et al., 2015; Wang et al., 2014; Xu et al., 2014; Yang et al., 2015; Zhang et al., 2015a; Zhang et al., 2015b).

Heavy metals are widespread contaminants in aquatic ecosystems, presenting particular features like high toxicity, multiple origins, refractory properties, and accumulative behavior that make them an environmental concern (Zhao et al., 2017). Heavy metal pollution can give rise to bioconcentration and bioaccumulation of toxic metals in aquatic species, resulting in long-term negative impacts for human and ecosystem health (Ip et al., 2007).

In the same way, microplastics (MPs) can cause significant environmental impacts, being ingested by marine organisms, especially filter feeders (Sleight et al., 2017; Egbeocha et al., 2018). MPs are plastic fragments smaller than 5 mm; they can be primary, manufactured for addition to certain products, or secondary, formed by physical, chemical and/or biological degradation from larger plastic residues in natural environmental processes (Wang et al., 2018).It is estimated that there are >250,000 tons of plastic in the global oceans (Eriksen et al., 2014). MPs can negatively impact animals through physical mechanisms (Browne et al., 2008), or by their physico-chemical properties (material, size, shape etc.) that can favor its toxicity, varying between several possible situations and interactions (Lithner et al., 2011), as well as via any externally adsorbed materials (Teuten et al., 2009).

Marine species can incorporate pollutants from bottom sediments, suspended particulate material, from the water column or food sources (Laffon et al., 2006). Thus biomonitoring can be an effective approach for evaluating the contamination. Bivalves are good sentinel organisms frequently used to evaluate marine environmental quality (Solé et al., 1994; Porte et al., 2000; Serafim and Bebianno, 2001). In addition, they stand out for their wide distribution in Brazil (native species) and in the world, vital ecological niches, susceptibility to pollutant absorption and close connection with marine predators and human health, as described by Li et al., 2019.

At the same time, exposure of aquatic organisms, such as bivalves to toxic contaminants could be a risk to human health if the contaminants are incorporated in the food chain (Lemiere et al., 2005). The aim of the study was to quantify heavy metals and microplastic particles in oysters (Crassostrea gasar) from sites distributed along the Paranaguá Estuarine System (PES) and its possible adsorption ratio.

The Paranagua Estuarine System (PES) is located on the north coast of the state of Paraná (SE Brazil) and consists of several regions and environments: to the west, the Bays of Paranaguá and Antonina, and to the north, the bays of Laranjeiras, Guaraqueçaba and Pinheiros and the inlets of Itaqui and Benito. The estuarine shore is occupied by extensive mangroves and hydrographical basins. In addition to the marine influence, the estuary receives considerable freshwater input from several rivers, primarily in the rainy season (summer). Two important harbors are installed in this area, Antonina and Paranaguá; the latter is one of the largest harbor for grain exportation in Latin America, reaching more than 8 million tons of shiploads in 2009 (Martins et al., 2010), posing risks to this bay. In addition, an artisanal fishery and aquaculture are two main economic and social activities in this region. However, the increase in urbanization and industrial activities in coastal regions have increased the level of pollutants in aquatic ecosystems (Pereira et al., 2006). This can lead to environmental contamination and cause health problems to humans and local fauna. Among some of the main pollutants in marine and estuarine environments, heavy metals play a prominent role and, more recently, microplastics have been shown to be important contaminants in aquatic environments (Barletta et al., 2019).

Section snippets

Methodology

Oysters were collected from 10 sampling stations along the PES (Fig. 1). These sites are representative of the estuary, being close to oyster producing communities, natural banks used for extraction and containing large human populations, with potential for high environmental pollution.

Ten oysters (n = 10) were collected at each location, which were called K1 to K10, totaling 100 organisms. In the laboratory, after collection, all oysters from each site were dissected and 30 mg of

Results and discussion

Some metals are considered essential elements since they participate in important physiological processes (Hogstrand and Haux, 2001). Others, however, are strong toxins causing dysfunctions in a variety of living organisms (Damek-Poprawa and Sawicka-Kapusta, 2003). Unfortunately, only Cr, Ni, Cu, Zn, As, Cd, Hg and Pb have maximum levels in tissues for human consumption established by Brazilian legislation (MS Ordinance n° 685/98 and Decree n° 55.871/1965). Metal levels determined in the

Conclusions

Oysters were confirmed as effective bioindicators of environmental quality. The results identified a potential risk to human health from oysters produced for consumption from PES, taking into consideration the high levels of heavy metals such as As and Zn. Likewise, MPs were found at all sampled locations, confirming the spread of this pollutant in the marine environment; its ability to bioaccumulate in oysters was also shown. However, it was not possible to establish a direct relationship

Funding

This research was funded by SNP (Secretaria Nacional de Portos).

Availability of data and material

Data will made available under request.

Code availability

Not applicable.

CRediT authorship contribution statement

Khauê Silva Vieira – Sampling, formal analysis, interpretation and discussion of data, preparation, creation and/or presentation of the published work, specifically up to the final version of the manuscript.

José Antônio Baptista Neto – Interpretation and discussion of data, writing the initial draft.

Miriam Araujo Carlos Crapez – Interpretation and discussion of data, writing the initial draft.

Christine Gaylarde – Interpretation and discussion of data, writing and review of the manuscript.

Bruno

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This research was funded by SNP (Secretaria Nacional de Portos). The authors are grateful to the Geology and Geophysics Department/LAGEMAR at UFF (Universidade Federal Fluminense), staff of the Central Laboratory of Electron Microscopy (LCME), Multiuser Laboratory of Biology Studies (LAMEB) and Laboratory of Biomarkers of Aquatic Contamination and Immunochemistry (LABCAI) at the Federal University of Santa Catarina (UFSC), Florianópolis, SC, Brazil for infrastructure and assistance with

References (100)

  • X. Guo et al.

    The chemical behaviors of microplastics in marine environment: a review

    Mar. Pollut. Bull.

    (2019)
  • L.A. Holmes et al.

    Adsorption of trace metals to plastic resin pellets in the marine environment

    Environ. Pollut.

    (2012)
  • L.A. Holmes et al.

    Interactions between trace metals and plastic production pellets under estuarine conditions

    Mar. Chem.

    (2014)
  • B. Hu et al.

    Occurrence and distribution of heavy metals in surface sediments of the Changhua River estuary and adjacent shelf (Hainan Island)

    Mar. Pollut. Bull.

    (2013)
  • C. Ip et al.

    Over one hundred years of trace metal fluxes in the sediments of the Pearl River estuary

    South China. Environ Pollut.

    (2004)
  • C.C. Ip et al.

    Trace metal distribution in sediments of the Pearl River estuary and the surrounding coastal area, South China

    Environ Pollut.

    (2007)
  • D. Joksimovic et al.

    Trace metal concentrations in Mediterranean blue mussel and surface sediments and evaluation of the mussels quality and possible risks of high human consumption

    Food Chem.

    (2011)
  • A. Karami

    Gaps in aquatic toxicological studies of microplastics

    Chemosphere.

    (2017)
  • B. Laffon et al.

    Monitoring of the impact of prestige oil spill on Mytilus galloprovincialis from galician coast

    Environ. Int.

    (2006)
  • G. Le Pennec et al.

    Evaluation of the toxicity of chemical compounds using digestive acini of the bivalve mollusc Pecten maximus L. maintained alive in vitro

    Aquat. Toxicol.

    (2001)
  • S. Lemiere et al.

    DNA damage measured by the single-cell electrophoresis (comet) assay in mammals fed with mussels contaminated by the “Erika” oil-spill

    Mutat. Res.

    (2005)
  • J. Li et al.

    Microplastics in mussels along the coastal waters of China

    Environ. Pollut.

    (2016)
  • J. Li et al.

    Microplastics in mussels sampled from coastal waters and supermarkets in the United Kingdom

    Environ. Pollut.

    (2018)
  • J. Li et al.

    Using mussel as a global bioindicator of coastal microplastic pollution

    Environ. Pollut.

    (2019)
  • A.S. Lino et al.

    Metal bioaccumulation in consumed marine bivalves in southeast Brazilian coast

    J. Trace Elem. Med. Biol.

    (2016)
  • V.F. Lira et al.

    Effects of barium and cadmium on the population development of the marine nematode Rhabditis (Pellioditis) marina

    Mar. Environ. Res.

    (2011)
  • D. Lithner et al.

    Environmental and health hazard ranking and assessment of plastic polymers based on chemical composition

    Sci. Total Environ.

    (2011)
  • D.R. Livingstone et al.

    Tissue and subcellular distribution of enzyme activities of mixed-function oxygenase and benzo[a]pyrene metabolism in the common mussel

    Sci. Total Environ.

    (1984)
  • J.C. Martinelli et al.

    Low incidence of microplastic contaminants in Pacific oysters (Crassostrea gigas Thunberg) from the Salish Sea, USA

    Science of The Total Environment.

    (2020)
  • C.C. Martins et al.

    Anthropogenic organic matter inputs indicated by sedimentary fecal steroids in a large south American tropical estuary (Paranaguá estuarine system, Brazil)

    Mar. Pollut. Bull.

    (2010)
  • A.R. McGoran et al.

    Presence of micropastic in the digestive tracts of the European flounder, Platichthys flesus, and the European smelt, Osmerus eperlanus, from the river Thames

    Mar. Pollut. Bull.

    (2017)
  • A. Naji et al.

    Microplastics contamination in molluscs from the northern part of the Persian Gulf

    Environ. Pollut.

    (2018)
  • R.S. Pazos et al.

    Microplastics integrating the coastal planktonic community in the inner zone of Río de la Plata estuary (South America)

    Environ. Pollut.

    (2018)
  • F.E. Possatto et al.

    Marine debris in a world heritage listed Brazilian estuary

    Mar. Pollut. Bull.

    (2015)
  • Y. Qiu et al.

    Sorption of polyhalogenated carbazoles (PHCs) to microplastics

    Mar. Pollut. Bull.

    (2019)
  • J.S. Silva-Cavalcanti et al.

    Microplastics ingestion by a common tropical freshwater fishing resource

    Environ. Pollut.

    (2017)
  • V.A. Sleight et al.

    Assessment of microplastic sorbed contaminant bioavailability through analysis of biomarker gene expression in larval zebrafish

    Mar. Pollut. Bull.

    (2017)
  • M. Solé et al.

    Mixed-function oxygenase system components and antioxidant enzymes in different marine bivalves: its relation with contaminant body burdens

    Aquat. Toxicol.

    (1994)
  • R.B. Suami et al.

    Assessment of metal concentrations in oysters and shrimp from Atlantic Coast of the Democratic Republic of the Congo

    Heliyon.

    (2019)
  • X. Sun et al.

    Retention and characteristics of microplastics in natural zooplankton taxa from the East China Sea

    Sci. Total Environ.

    (2018)
  • J. Teng et al.

    Microplastic in cultured oysters from different coastal areas of China

    Sci. Total Environ.

    (2019)
  • S. Venkatramanan et al.

    Evaluation of geochemical behavior and heavy metal distribution of sediments: the case study of the Tirumalairajan river estuary, southeast coast of India

    International Journal of Sediment Research.

    (2015)
  • J. Wang et al.

    Spatial variation, environmental assessment and source identification of heavy metals in sediments of the Yangtze River estuary

    Mar. Pollut. Bull.

    (2014)
  • H. Wang et al.

    Spatial variation, environmental risk and biological hazard assessment of heavy metals in surface sediments of the Yangtze River estuary

    Mar. Pollut. Bull.

    (2015)
  • X. Wang et al.

    Metal concentrations in the mussel Bathymodio lusplatifrons from a cold in the South China Sea

    Deep-Sea Res. I

    (2017)
  • C.C. Wessel et al.

    Abundance and characteristics of microplastics in beach sediments: insights into microplastic accumulation in northern Gulf of Mexico estuaries

    Mar. Pollut. Bull.

    (2016)
  • Y. Xu et al.

    The source of natural and anthropogenic heavy metals in the sediments of the Minjiang River estuary (SE China): implications for historical pollution

    Sci. Total Environ.

    (2014)
  • X. Yang et al.

    Spatial distribution and sources of heavy metals and petroleum hydrocarbon in the sand flats of Shuangtaizi Estuary

    Bohai Sea of China. Mar Pollut Bull.

    (2015)
  • H. Zhang et al.

    Sorption of fluoroquinolones to nanoplastics as affected by surface functionalization and solution chemistry

    Environ Poll.

    (2020)
  • X. Zhu et al.

    Bioaccumulation of microplastics and its in vivo interactions with trace metals in edible oysters

    Mar. Pollut. Bull.

    (2020)
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