Assessment of metal concentration in Goniopsis cruentata (Latreille, 1803) (Decapoda, Grapsidae) from two Brazilian mangroves under different anthropogenic influences

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Highlights

  • Mangrove sediments are frequently contaminated with metals and may become associated with crabs during their feeding.

  • Concentrations in the sediment were below the metal levels established for TEL and PEL at both sites.

  • As, Cu, Cr Pb and Zn levels in crab muscle were above what is considered safe for human health.

  • Highest concentrations of metals occurred in the hepatopancreas, except for Cu (gills) and Zn (muscle).

Abstract

The red mangrove crab is an omnivorous endemic species that lives in mangrove areas throughout the Brazilian coast and is a potential bio-accumulator of metals. These ecosystems are usually located in regions with intense anthropic activity. They also have physicochemical characteristics such as fine grained sediments, that favor the stabilization of metal contaminants. This study quantified the accumulation of seven metals (As, Cd, Cu, Cr, Ni, Pb and Zn) in the sediment and in three tissues (gills, hepatopancreas and muscle) of Goniopsis cruentata that were collected during different periods from two mangrove areas. These mangroves, Cardoso and São Vicente Islands on the coast of the State of São Paulo, experience different anthropogenic influences. The concentrations of metals in sediments were below the established metal concentrations provided by sediment quality guidelines (TEL and PEL) at both sites, indicating no adverse effects on the local biota. The highest concentrations of toxic elements (As, Cd and Pb) were found in the individuals from Cardoso Island, and significant differences were found among the analyzed factors (site, season and sex). The relative concentrations of metals among the tissues exhibited the same pattern, i.e., gills > hepatopancreas > muscle, except for Zn, with the highest concentrations recorded in muscle tissue. The levels of metals in muscle tissue were above the maximum permissible limits established for food by Brazilian legislation.

Introduction

The mangrove ecosystem is considered one of the most threatened environments on the planet because it is generally associated with areas of intense urban activity, such as industrial complexes, ports and large cities (Elliott and Whitfield, 2011). Moreover, mangroves have physicochemical characteristics such as high organic content, fine grained sediment and reducing conditions, which favor stabilization of contaminants due to the retention behaviors of organic and inorganic materials, making the mangrove ecosystem an important reservoir of metals (Vannucci, 2001). Metals are naturally occurring compounds, but become contaminants if their concentrations are elevated above natural background levels (Masindi and Muedi, 2018), such as will occur if anthropogenic activities introduce them in large quantities.

Metals are known for their high degree of toxicity and persistence in the environment (Ahearn et al., 2004, Rainbow and Black, 2005, Rainbow, 2007); they can accumulate in crustacean tissues in higher concentrations than in the water column and sediments (Rainbow, 2007). Some of these elements are considered non-essential, such as Hg, Pb and Cd, and have a high degree of toxicity even at low concentrations; other elements are essential with an important role in animal metabolism, such as Cu and Zn, but become toxic at high concentrations (Eisler, 2010).

Understanding the levels of these elements has been useful to establish parameters of contamination in natural environments (Rainbow, 2007, Luoma and Rainbow, 2008). In Brazil, several studies have described the effects of high levels of metals on crustaceans (Harris and Santos, 2000, Pinheiro et al., 2012, Álvaro et al., 2015, Almeida et al., 2016, Duarte et al., 2016, Duarte et al., 2017, Banci et al., 2017). The bioavailability of metals in marine invertebrates can be influenced by several factors, such as biological (e.g., size, age, diet and sex) (Rainbow, 1985, Jeckel et al., 1996, Chen et al., 2005, Franchi et al., 2011), seasonal (Beltrame et al., 2010, Beltrame et al., 2011) and sampling location (Álvaro et al., 2015, Ortega et al., 2017), and these factors affect the development of strategies and physiological responses.

Crabs possess a variety of cellular detoxification mechanisms and are able to store toxic metals in intracellular organelles, such as lysosomes and in the hepatopancreas, which is an important detoxification organ. Crabs also have intracellular scavenging mechanisms, including high affinity binding sites on low molecular weight proteins called metallothioneins, followed by their elimination through the lysosomal endomembrane system (Ahearn et al., 2004), or compartments in granules formed by the hepatopancreas, which is the main organ for detoxification (Corrêa-Júnior et al., 2000). The gills are selective organs that act between the internal and external environments and are the first organs affected by pollutants when water is contaminated (Ortega et al., 2014).

The red mangrove crab Goniopsis cruentata (Latreille, 1803), commonly known as aratu, maria-mulata or red aratu, is a semi-terrestrial species common in Brazilian mangroves and can be found in the eastern Atlantic from Senegal to Angola and the Cape Verde Islands, and in the western Atlantic from Florida, the Gulf of Mexico, Bermuda, Antilles, Guianas and Brazil (Melo, 1996). This species plays an important ecological role in the mangrove ecosystem, affecting soil biogeochemistry, decomposition rates and nutrient cycling (Kristensen, 2008, Lima-Gomes et al., 2011). This species also serves as a fishing resource for the traditional communities located along the northeastern coast of Brazil (Santos et al., 2001, Santos and Botelho, 2002, Moura and Coelho, 2004, Pinheiro et al., 2016). G. cruentata is not currently economically exploited along the southeastern coast of Brazil, but may be in future considering the increasing exploitation of other crab species populations in the region (Botelho et al., 2004).

The Brazilian Ministry of the Environment estimates that 3,000 tons of liquid pollutants, including industrial waste that contains metals, are released into the sea daily, posing a major threat to mangroves and estuaries (MMA, 2002). A review of pollutants on the coast of São Paulo revealed the presence of high concentrations of metals and organic contaminants in the region of Baixada Santista, São Vicente when compared to levels recorded in the extreme southern region of the coast near Cardoso Island and Cananeia, Brazil (Duarte et al., 2016).

Chemical contamination originating from sediment and the consumption of small organisms can induce genetic alterations in predators, causing physiological damage and ecological imbalance (Kirschbaum et al., 2009). Pinheiro and Toledo (2010) recorded a malformation in a specimen of the species Ucides cordatus which was potentially caused by stress from high levels of environmental pollution. An increase in the number of pollution studies that analyze ecological risks and their consequences for estuarine life has resulted from indications such as these.

Considering the potential bioavailability of metals in these ecosystems, this study aimed to quantify the levels of As, Cd, Cr, Cu, Ni, Pb and Zn in three tissues (gills, hepatopancreas and muscle) of the red mangrove crab G. cruentata. The concentrations of metals in surface sediment samples from two mangrove areas (Cardoso and São Vicente Island, coast of São Paulo) with different levels of impact were evaluated as a way of assessing the levels of local contamination and any risk of using the species as a potential fishing resource in the region. The influence of factors such as sex and seasonality on the concentration of metals was also evaluated.

Section snippets

Study area

The coast of São Paulo has approximately 662 km of coastline, with the coast divided into three sectors: north, south and central (metropolitan). The latter is known as the “Metropolitan Region of Baixada Santista”, comprising a densely urbanized area of great economic importance, mainly due to the presence of the Port of Santos, the largest port in Latin America (Harari and Gordon, 2001). The Santos-São Vicente Estuarine System represents one of the most notable examples of environmental

Metal concentrations in sediments

The mean concentrations (mg kg−1) of Cd, Cr, Cu, Ni, Pb and Zn in the sediment samples from both study sites (Cardoso Island and São Vicente) are shown in Table 1. Significant statistical differences were found between sites for all elements (F=22.92; p<0.0001); however, there were no differences between seasons (F=1.04; p=0.427). The seasonal distribution of metals in the sediment showed a similar result in all periods of the study.

The highest mean levels of each element were recorded in São

Discussion

All measured metal concentrations in sediment samples from both sites were below the TEL and PEL, and no adverse effects on the biota should be expected. These results differ from those found by Banci et al. (2017), whose concentrations in surface sediment from São Vicente were slightly lower: Cd: 0.10 (± 0.02) mg kg−1; Cr: 7.07 (± 0.45) mg kg−1; and Pb: 10.33 (± 0.56) mg kg−1; the results for Cu, 5.81 (± 1.28) mg kg−1, were similar to those found in the present study. These differences may be

Conclusion

The concentrations of metals in the sediment were below the values established for TEL and PEL at both sites, indicating that adverse effects should not be expected for local biota. For G. cruentata, the concentrations of metals in the individuals sampled in both regions indicated that the species was unfit for human consumption due to the high levels of contamination found in all tissues that were analyzed. In general, the highest concentrations of metals occurred in the hepatopancreas, which

CRediT authorship contribution statement

Vedolin, M.C. conceived of the presented idea and developed the field and laboratory work. Trevizani, T.H. and Angeli, J.L.F. verified the analytical methods. Petti, M.A.V. and Figueira, R.C.L. encouraged the principal author to investigate about heavy metals on the crab specie and supervised the findings of this work.

All authors discussed the results and contributed to the final manuscript. Vedolin, .C. and Trevizani, T.H. carried out the experiment. Petti, M.A.V. and Figueira, R.C.L.

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

Financial support for this study was mainly provided by CNPq, Brazil [165469/2015-3] and technical support from Oceanographic Institute of University of São Paulo, Brazil (IOUSP).

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