Bioaccumulation and retention kinetics of trace elements in the horse mussels Modiolus micropterus exposed to different environmental conditions

https://doi.org/10.1016/j.etap.2021.103692Get rights and content

Highlights

  • Limited bioaccumulation study of heavy metal and radionuclides in Jakarta bay.

  • Benthic mussels can be used for bio indicator of Zn and Cs-137.

  • Bioaccumulation studies are useful for making environmental regulations.

  • Bioaccumulation studies were performed using a radiotracer.

Abstract

Bioaccumulation studies of Zn and 137Cs by the horse mussel (Modiolus micropterus) were conducted in a laboratory that used radiotracer. The study has been carried out on the effect of cesium and zinc concentrations and the effect of sea seawater salinity on the ability of M. micropterus to accumulate these two contaminants. The uptake of Zn and Cs according to the one-compartment model and the experiment was carried out until the steady-state conditions were reached. The concentration factor at steady-state Zn is 31.94–45.54 mL. g−1 and 23.22–33.26 mL. g−1 which are influenced by the concentration and salinity of seawater, respectively. The concentration factor of 137Cs at steady-state conditions due to changes in concentration and salinity is 3.34–7.55 mL. g−1 and 4.23–9.66 mL. g−1, respectively. The release rates of Zn were 30–47 % and 39–49 % at various concentrations and salinity. The depuration rate from concentration reaching 60 % and salinity at ranges 43–52 % was observed within 10 days after exposure. On the other hand, the release rates of 137Cs were 60 % and 43–52 % at various changes in the concentration and salinity of seawater

Introduction

Coastal waters are subject to several significant pressures; among them, high urbanization and industrial production associated with chemical pollution are of major concern (Giarratano et al., 2010). Threats to coastal ecosystems are a global problem that increasingly requires efficient monitoring. Among the approaches used to study contamination of the environment (Hédouin et al., 2010; Phillips, 1977; Danis et al., 2004), shellfish species such as mussels are widely used as biomonitoring program and excellent sentinels since they bioaccumulate these substances through their digestive tracts (substances adsorbed onto particles) and gills (dissolved substances) (Norambuena-Subiabre et al., 2016; Andral et al., 2011; Baumard et al., 1998; Gomez et al., 2012).

The horse mussel (Modiolus micropterus), lives separately in surface sediments. In Indonesia, these mussels live attached to the large seagrass rhizomes of Thalassia hemprichii and Enhalus acoroides (Asmus and Asmus, 2012). This mussel is easily identified in the field and widely cultivated in Indonesia's Jakarta Bay. While bivalves, in general, accumulate trace metal contamination, the horse mussel has been studied very little and may become a useful indicator of metal bioaccumulation and become a candidate for more detailed investigations (Genta-Jouve et al., 2012).

Studies related to contaminant bioaccumulation by Modiolus micropterus are very limited. The activity of metabolic enzymes of oxidative stress, and expression of heat shock protein (HSP) have been studied (Lesser and Kruse, 2004). The identification of bivalves in the Tanjung Balai North Sumatra, Indonesia has been conducted to make an inventory of Moodiolus micropectus as one of the bilalves found in the area (Sari et al., 2014). Modiliolus micropterus has also been studied in its accumulation of Hg and radionuclide content (Ramakritinan et al., 2012; Dovzhenko et al., 2005). Bioaccumulation studies of Zn and 137Cs by mussels especially in Jakarta Bay have not been carried out.

Ecologically, Jakarta Bay is under continuous pressure from the entry of chemical, biological, and radioactive contaminants from land and marine sources which result in environmental degradation (Prihatiningsih et al., 2016). A serious threat to the global environment is a heavy metal which is one of the chemical contaminants (Burger et al., 2007; Hao et al., 2019; Wang et al., 2018). Bioconcentration factor (BCF) is the basis for the ability of organisms to uptake and excrete heavy metals, which was significant for heavy metals in seawater more bioavailable higher than in sediment (Hao et al., 2019; Yang-guang et al., 2018; Jiang et al., 2015; Kwoczek et al., 2006; Gu et al., 2017; Liu et al., 2015). Human health can seriously be affected by metal bioaccumulation in marine organisms (Hao et al., 2019) in terms of both qualities of longevity and life. Heavy metals such as Zinc (Zn), are one of the most common elements in the Earth's crust. Zinc is an essential element for health at low daily doses in organisms (Hao et al., 2019) and it can be toxic to organisms at high concentrations including aquatic organisms (McDonald et al., 2020). The 137Cs radionuclide is substantially soluble in seawater so ocean currents and water masses can carry them over great distances (Suseno and Prihatiningsih, 2014). The source of 137Cs in the Jakarta Bay comes from global ocean flow into Indonesian marine waters, global fallout and a proportion originate from a nuclear facility in Serpong, South Tangerang, Indonesia (Suseno et al., 2018).

Many studies of the bioaccumulation of 137Cs by marine organisms have been conducted associated with releases and accidents. The results of this study provide some information regarding the accumulation capacity of 137Cs by fish and bivalves (Pouil et al., 2017; Kawai et al., 2014) using metrics such as field ecological half-life or concentration factors (Metian et al., 2016). Cesium-137 is a radioisotope that is of particular interest because of its relatively long half-life, its residence time in the water, and its considerable abundance. The most important route of this radioisotope bioaccumulation by various marine invertebrates (shrimp, zooplankton, and fish larvae, and some mollusks) is via the water pathway (Thomas and Fisher, 2019).

This research aimed to study the bioaccumulation of Cs and Zn to mussels (Modiolus Micropterus) from Jakarta Bay. It is located in the Tangerang region of North Banten Province with abundant fishery products, one of which is shellfish. For this purpose, we conducted experimental uptake and depuration of 137Cs by horse mussel. The influence of abiotic factors (such as the concentration of contaminants or salinity) that are effective in the ability of this mussel to accumulate 137Cs were also characterized (Kuranchie-Mensah et al., 2018). This work will be investigated by a high-resolution γ spectrometry system consisting of High-purity germanium (HPGe) detectors. Recent reviews on the topic of radionuclide and heavy metal transfer in marine organisms have suggested the importance of obtaining more data on bioaccumulation by tropical species to make comparisons valid on a global scale (Ansoborlo and Adam-Guillermin, 2012). The two contaminants were selected based on their essentiality (Zn) and non-essentiality (Cs) as well as a comparison of their contrasting chemical properties.

Section snippets

Materials and methods

The methods of this research refer to Hedouin et al. (2010) and Kuranchie-Mensah et al., 2018 with several modifications (Hédouin et al., 2010; Kuranchie-Mensah et al., 2018)

Results and discussion

Bivalve species, such as Modiolus micropterus is one type of seafood in Indonesia. On the other hand, various contaminants can be accumulated by bivalves (Suseno and Prihatiningsih, 2014). Species have no mortality during acclimatization, bioaccumulation and, depuration experiments. The uptake kinetics of 65Zn and 137Cs in the horse mussel are shown in Fig. 1, Fig. 2, Fig. 3, Fig. 4, Fig. 5, Fig. 6, Fig. 7, Fig. 8 and Table 1. In general, the accumulation of contaminants is caused by the uptake

Conclusion

The biokinetics of uptake and depuration Zn and 137Cs into organisms such as appear to be important to determinate the bioaccumulation characteristic of marine species such as bivalves and to make the validation of their act as a biomonitor, which reflects an integrated time picture of the state of environmental contamination. Our results show that Modiolus micropterus shells quickly and efficiently accumulate Zn and Cs. This suggests that important information about the contamination of metal

CRediT authorship contribution statement

Budiawan Budiawan and Heny Suseno: are the main contributor on this paper due to their expertise and knowlagde.

Authorship

BB and HS are the main contributor on this paper.

Declaration of Competing Interest

The authors report no declarations of interest.

Acknowledgments

This research was founded by Faculty of Mathematics and Science, Universitas Indonesia and Center Technology for Radiation Safety and Metrology - National Nuclear Energy Agency and The authors is grateful for the National Nuclear Energy Agency for the support provided to its Marine Ecology Laboratories and skillful technical assistance.

References (43)

  • A. Krężel et al.

    The biological inorganic chemistry of zinc ions

    Arch. Biochem. Biophys.

    (2016)
  • H. Kuranchie-Mensah

    Allometric relationship in the bioaccumulation of radionuclides (134Cs & 241Am) and delineation of contamination pathways (food and seawater) in bloody cockle Anadara senilis using radiotracer techniques

    J. Environ. Radioact.

    (2018)
  • M.P. Lesser et al.

    Seasonal temperature compensation in the horse mussel, Modiolus modiolus: metabolic enzymes, oxidative stress and heat shock proteins

    Compar. Biochem. Physiol. - Mol. Integr. Physiol.

    (2004)
  • M. Metian

    Interspecific comparison of Cd bioaccumulation in European Pectinidae (Chlamys varia and Pecten maximus)

    J. Exp. Mar. Biol. Ecol.

    (2007)
  • M. Metian

    Differential bioaccumulation of 134Cs in tropical marine organisms and the relative importance of exposure pathways

    J. Environ. Radioact.

    (2016)
  • I.H. Ni et al.

    Influences of salinity on the biokinetics of Cd, Se, and Zn in the intertidal mudskipper Periophthalmus cantonensis

    Chemosphere

    (2005)
  • L. Norambuena-Subiabre et al.

    Uptake and depletion curve of Diflubenzuron in marine mussels (Mytilus chilensis) under controlled conditions

    Aquaculture

    (2016)
  • D.J.H. Phillips

    The use of biological indicator organisms to monitor trace metal pollution in marine and estuarine environments-a review

    Environ. Pollut. (1970)

    (1977)
  • S. Pouil

    Comparative study of trophic transfer of the essential metals Co and Zn in two tropical fish: a radiotracer approach

    J. Exp. Mar. Biol. Ecol.

    (2017)
  • W.R. Prihatiningsih

    Bioaccumulation and retention kinetics of cesium in the Milkfish Chanos chanos from Jakarta Bay

    Mar. Pollut. Bull.

    (2016)
  • A.M. Rodriguez y Baena

    A single vs. double spike approach to improve the accuracy of 234Th measurements in small-volume seawater samples

    Mar. Chem.

    (2006)
  • View full text