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IJERPHInternational Journal of Environmental Research and Public Health
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  • Commentary
  • Open Access

25 March 2021

24 Pages

A Commentary on the Use of Bivalve Mollusks in Monitoring Metal Pollution Levels

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1
Department of Biology, Faculty of Science, Universiti Putra Malaysia, Serdang 43400, Selangor, Malaysia
2
Shrimp Research Center, Iranian Fisheries Science Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Bushehr 75169-89177, Iran
3
Faculty of Health and Life Sciences, Inti International University, Persiaran Perdana BBN, Nilai 71800, Negeri Sembilan, Malaysia
4
Indian River Research and Education Center, IFAS, University of Florida, Fort Pierce, FL 34945, USA
Int. J. Environ. Res. Public Health2021, 18(7), 3386;https://doi.org/10.3390/ijerph18073386
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Abstract

The objective of this commentary is to promote the use of bivalves as biomonitors, which is a part of the continual efforts of the International Mussel Watch. This commentary is an additional discussion on “Bivalve mollusks in metal pollution studies: From bioaccumulation to biomonitoring” by Zuykov et al., published in Chemosphere 93, 201–208. The present discussion can serve as a platform for further insights to provide new thoughts and novel ideas on how to make better use of bivalves in biomonitoring studies. The certainty of better and more extensive applications of mollusks in environmental monitoring in the future is almost confirmed but more studies are urgently needed. With all the reported studies using bivalves as biomonitors of heavy metal pollution, the effectiveness of using Mussel Watch is beyond any reasonable doubts. The challenge is the development of more accurate methodologies for of heavy metal data interpretation, and the precision of the biomonitoring studies using bivalves as biomonitors, whether in coastal or freshwater ecosystems. Lastly, inclusion of human health risk assessment of heavy metals in commercial bivalves would make the research papers of high public interest.

1. Introduction

Firstly, the well-written review paper published by Zuykov et al. [1] promoting the use of bivalves as biomonitors is focused on and discussed in the present commentary paper. As of January 2021, this paper had been cited by 165 papers based on Google Scholar. This monitoring paper using bivalves is a part of a continual effort of the International Mussel Watch. This mussel monitoring work should have been highly commended and supported from its inception when it was suggested by Goldberg [2] and should continue to be for educational purposes. This is because of the fact that the pollutant levels in bivalves will greatly affect human health.
We must say that it is not our intention to offend the good researchers in the paper by Zuykov et al. [1], but our honest comments are based on science. As researchers working on biomonitoring studies using mussels since 1998, we want to humbly comment and add more discussion on the above review paper, based on the following highlighted points of view as presented the paper.
  • The uses of bivalves as biomonitors of metal pollution are primitive methods.
  • The use of shells to construct pollution history blueprint is futile.
  • There has not been any documented evidence of severe health effects of bivalves due to metal accumulation.

2. Comments and Discussions

Two of the specific goals of the paper by Zuykov et al. [1] were to (1) “discuss the biomonitoring of metal pollution using bivalves”, soft tissues and shells as a mean of environmental “health monitoring”, and (2) “reveal additional information of metal pollution in aquatic environments based on the observation of the internal shell surface through scanning electron microscope”. However, these objectives were not answered and not actually summarized or briefly discussed in the abstract.

2.1. The Uses of Bivalves as Biomonitors of Metal Pollution Are Primitive Methods

It seems to the general readers that the biomonitoring of metals using bivalves is not effective and is an old research method. We disagree with this highlighted point because there has been an influx of reported studies, before, now and expectedly in the future too, using bivalves for pollution studies. As reviewed in Table 1, many such studies can be found in different countries up until January 2021. In our view, we would not say “primitive” since this could totally discourage the use of bivalves in metal pollution monitoring and funding for such studies would not be continued. We think, besides bioaccumulation data, the effectiveness of using identified bivalves for the biomonitoring of metal pollution for spatial distribution and comparison should be improved upon and the accuracy enhanced, in future studies.
Table 1. A review on the use of bivalves’ soft tissues for metal pollution studies from some of the available literature.
In fact, Zuykov et al. [1] made a substantial, careful and excellent review on the use of bivalve soft tissues and shells in biomonitoring studies from numerous papers. Even similar early papers by Boening [3], Yap et al. [4] and Yap [5] have given suggestions for biomonitoring assays using marine mussels. This trend continues in recent papers such as Nędzarek et al. [6] and Wepener and Degger [7]. All of this clearly shows the potential of mollusks as sentinel organisms of heavy metal pollution for future studies. In particular, Yap [5] and Yap et al. [8] proposed that the recommended criteria for marine mussels could be applied to other mollusk species, establishing them as good biomonitors of heavy metal pollution. None of these papers mentioned that “the biomonitoring work is not far advanced”. Therefore, in our opinion, the uses of bivalves as biomonitors of metal pollution are far reaching methods instead of being primitive.
The paper entitled “From bioaccumulation to biomonitoring” is somewhat confusing to the readers too. However, when the abstract is carefully looked into, “biomonitoring” means “estimation of environmental quality”. In fact, biomonitoring is better explained as “regular and systematic use of living organisms to evaluate changes in environmental or water quality that involves repetitive measurements of pollutants/chemicals”, which is central to aquatic toxicology and ecotoxicology. In the science of analytical chemistry, biomonitoring is the estimation of the body burden of poisonous synthetic compounds, elements, or their metabolites in bioorganic substances [98].
Before we can better estimate the environmental quality, we think the current challenges now are to enhance the precision of the biomonitoring studies using bivalves as biomonitors, whether in coastal or freshwater ecosystems. These challenges have been little discussed in the recent literature (Table 1). The metal bioaccumulation data in bivalves could be influenced by several abiotic and biotic factors. For example, the abiotic (such as pH, salinity, etc.) and the biotic (sizes, gender, genetic differentiation, predation, competition) factors could simply alter the metal bioaccumulation data in the body tissues of the bivalves [99].
Based on the title of the paper again, most ecotoxicologists will understand that the use of bivalves for biomonitoring purposes is of high novelty. However, bivalves have been widely employed and recognized as good biomonitors of four major collective pollutants—namely, halogenated hydrocarbons, transuranics, heavy metals and petroleum, as mentioned in the Mussel Watch Program [2]. This is because mussels have many of the important characteristics of good biomonitors [100,101] of coastal pollution. According to Farrington et al. [101], bivalves are widely distributed in coastal waters across the globe, are sessile in nature, are capable of accumulating pollutants at high concentrations (by factors of 103 to 105), seem to be unaffected by pollutants, are important seafood products heavily consumed in certain parts of the world and therefore can be a risk to human health. For Perna viridis particularly, extensive studies had been reported from the Asia-Pacific coastal regions [102,103]. From at least 65 of the high impact publications as seen in Table 1, four patterns can be deduced.
Firstly, publications on metal studies in mussels have been consistently and widely accepted worldwide in more than 50 countries around the world’s coastal regions, as summarized in Table 1, spanning from the 1970s until January 2021.
Secondly, there have been continuous efforts made and research grant allocations given to study heavy metal levels in bivalve mollusks in both marine and freshwater environments, but mainly in marine mussels, ever since the introduction of the famous International Mussel Watch, initially proposed by Prof. Goldberg [2]. This shows that metal pollution studies using mussels are not only truly scientific research studies based on biomonitoring, but they have also triggered other newly emerging scientific studies and topics.
Thirdly, the summary in Table 1 highlights that biomonitoring studies using mussels occur in developed, developing and underdeveloped countries all around the world. This greatly signifies that Mussel Watch is a cost-effective study and the idea has spread in a very positive and fruitful manner in all coastal areas around the world. The benefits include developing expertise in the areas of ecotoxicology, biology and environmental sciences, which eventually lead to opportunities for training postgraduate research students.
Fourthly, the common heavy metals such as Hg, Cd, Cu, Pb and Zn have always been focused upon with Ag, Al, As, Ba, Ni, Co, Cr, Fe, Mn, Se, Sr, Sn, Ti and V. In fact, the biomonitoring studies using bivalves have been expanded to more metals or elements including rare earth elements (Table 1). Therefore, if biomonitoring studies using mussels are “not far advanced”, then this work is a futuristic study that is influential in many regions around the world with its ever-expanding trends, although it is traditional in its origins and ideas.

2.2. The Use of Shells to Construct Pollution History Blueprint Is Futile

We have conducted a comprehensive review covering papers published up until January 2021 on the use of bivalves’ shells for the biomonitoring of metals. In addition, based on the review presented in Table 2, more related studies give evidence that such studies are continuing now and in the future. The main reason for this is because shells have potential for biomonitoring metal pollution, and it is believed that they can be reconstructed to reflect the metal pollution history. This challenge remains.
Table 2. A review on the use of shells of bivalves in metal pollution studies from some of the available literature.
The original idea of using the shell as a reliable biomonitoring material for the reconstruction of pollution history (see [133,134,135,136,137,138]) is acceptable and is believed to be workable and reliable when compared to the use of soft tissues. This is the main reason why so many researchers conducted such related studies using molluscs’ shells for the biomonitoring of metal pollution, to compare the current with the past history of metal bioaccumulation in bivalve shells as reviewed in Table 3. The reason why we compared the previously collected shells with the current ones is because we can logically establish the past pollution history as shells can be easily stored without having to be kept in a freezer (Table 3).
Table 3. A review on the use of bivalves’ biomarkers in metal pollution studies on bivalves from some of the available literature.
Overall, researchers are trying to provide more data and evidence, but the reconstruction of pollution history using shells remains a big challenge. Therefore, while we wait for more evidence to prove the positive usage of mollusc shells for elucidating pollution history, we think it is premature to say “Shells cannot be reliably used for the reconstruction of the pollution history”. In fact, almost all the papers reviewed by Zuykov et al. [1] concluded on the positive use of bivalves’ shells for biomonitoring of metal pollution and none stated the contrary. Rather, we think more studies are needed to establish the use of bivalves’ shells as good biomonitors and to reconstruct the pollution history of heavy metals.

2.3. There Has Not Been Any Documented Evidence of Severe Health Effects of Bivalves Due to Metal Accumulation

If the paper is only based on the reviewed literature, we disagree with the statement that “There are no effects of high metal bioaccumulation on the health status of bivalves”. In fact, a number of biomarkers have been used to show the health effects due to metal bioaccumulation in the mussels and these have also been evidently proven (Table 2). For example, the condition index (CI) of bivalves has been widely used as a health status measure in response to high metal bioaccumulation in bivalves due to pollution effects [139]. Unless there are other major factors, the metal levels in the body tissues and the CI of bivalves are negatively correlated. Based on their studies, de los Ríos et al. [140] reported the detrimental effects on mussels’ health from metals and xenoestrogenic endocrine disruptors found in some discharges. Signa et al. [119] reported that a lower condition index and phospholipids, as well as higher total and neutral lipids in mussels from Augusta, indicated the occurrence of physiological and biochemical stress responses to metal exposure and accumulation.
Riveros et al. [141] measured cellular biomarkers (the levels of vacuole formation and the amount of lipofuscin granules in the digestive system as well as lysosomal stability in haemocytes) in the mussel Perumytilus purpuratus from the intertidal zones of San Jorge Bay, Antofagasta, Chile. Al-Subiai et al. [143] concluded based on the multibiomarker approach using Mytilus edulis that a visible relationship between genotoxicity and higher-level effects was present and this could be used to determine various short- and long-term toxic effects of Cu. Marigomez et al. [144] reported that biomarkers in depicted site-specific profiles served as essential diagnostic tools for health assessments of metal pollution not just of mussels but of the marine ecosystem as well. Their study supported a combined use of both caged and native mussels in highly polluted areas to monitor the biological effects of pollution in mussels through the integrative biomarker approach. Brooks et al. [150] highlighted the biological effects of pollutants on the blue mussel (Mytilus spp.) to evaluate the effluents discharged from the Sydvaranger mines. The results of the integrated biological responses were in line with the source of pollution judging by the distance and location between the mussels and the discharge outlet and the expected exposure to the mine effluents. González-Fernández et al. [151] concluded that the vast variability of the population of the mussel, Mytilus galloprovincialis, caused by environmental factors such as food availability in a certain monitoring program might conceal the effects of pollutants on the biomarkers. Chandurvelan et al. [152] reported that the specific tissue or the whole organism response of Perna canaliculus towards metal pollutants reveals crucial information on the biological stress responses, denoting the importance of such measurements in biomonitoring programs in New Zealand. Giarratano et al. [147] reported that the gill of the mussel Aulacomya atra is an actively proliferating tissue and is the first target of contaminants (Fe, Al, Zn, Cu, Cd and Pb) present in the water, so that changes in its antioxidant system can provide an earlier warning signal than changes in other tissues. Lekube et al. [148] concluded that cellular biomarkers in Mytilus galloprovincialis were extremely sensitive and quick to respond to changes in environmental pollutants such as heavy metals. The results obtained by Tsangaris et al. [62] confirmed the usefulness of the integration of biological effect measurements and chemical analysis in Mytilus galloprovincialis for the assessment of chemical contamination including those by Cu, Ni, Fe and Zn in coastal waters. Other studies using biomarkers as evidence to show the effects of accumulated metals in relation to the health of the mussels investigated are shown in Table 3.
According to Lam and Gray [175], biomarkers can be used for the quantitative determinations of physiological and biological changes that are observed in cells, body fluids, tissues or organs of an organism. These serve as indicators of exposure to xenobiotics and their effects. Therefore, the accumulated metals on the health of bivalves can be reflected by looking into the biomarkers of the mussels.

3. Human Health Risk Assessment of Heavy Metals in the Bivalves

Table 4 shows a review on the human health risk assessments of heavy metals in bivalves from some available literature. With the increasing trends of anthropogenic inputs into aquatic ecosystems, the commercial shellfish from these areas are of much public concern. Therefore, from Mussel Watch monitoring to human health risk assessment of heavy metals are of high significance [176,177]. It seems that with heavy metal data in the bivalves without the human health risk assessment of the heavy metals would make the whole research finding of low novelty.
Table 4. A review on the human health risk assessments of heavy metals in bivalves from some of the available literature.

4. Conclusions

With all the reported studies using bivalves as biomonitors of heavy metal pollution, the effectiveness of using Mussel Watch is beyond any reasonable doubts. The challenge is on the development of more accurate methodology of heavy metal data interpretation and the precision of the biomonitoring studies using bivalves as biomonitors, whether in coastal or freshwater ecosystems. Such ideas have been marginally proposed in the literature [189,190]. In addition, human health risk assessment of heavy metals in commercial bivalves will be of much public interest. Therefore, inclusion of consumer perspectives on the heavy metal data is of high importance. Lastly, the Mussel Watch approach could be proposed as Crop Watch in studies of ecotoxicological genetics [191].
This commentary is an additional discussion on “Bivalve mollusks in metal pollution studies: From bioaccumulation to biomonitoring” by Zuykov et al. [1]. It is hoped that this communication paper will serve as a platform for further discussion that can provide new thoughts and novel ideas on how to make better use of bivalves, both marine and freshwater, in biomonitoring studies. It is certain that more future studies using bivalve mollusks as biomonitors of pollution are much needed.

Author Contributions

Conceptualization, C.K.Y.; methodology, C.K.Y.; validation, M.S.; formal analysis, C.K.Y.; investigation, C.K.Y.; resources, C.K.Y.; data curation, C.K.Y.; writing—original draft preparation, C.K.Y.; writing—review and editing, M.S., S.A.A.-S., W.H.C., K.W.W., and K.A.A.-M. All authors have read and agreed to the published version of the manuscript.

Funding

This study was partially funded by UPM Journal Publication Fund.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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