A Critical Assessment of Microplastics in Molluscan Shellfish with Recommendations for Experimental Protocols, Animal Husbandry, Publication, and Future Research

Abstract

Microplastics (MP) are a contaminant of emerging concern and, as such, there has been a rush to action and publication. Over the past two decades, this haste has resulted in a chaotic and cluttered literature rife with inappropriate methodologies, poor experimental protocols, misinterpreted results, overstated significance, and subsequent damaging media stories. This review provides a critical assessment of the current scientific literature on interactions between particle-feeding molluscs and MP and their purported impacts (>750 publications), and recommendations for future efforts. Experimental studies were critically assessed and assigned scores ranging from 0 to 2 as indicators of their veracity. The mean ratio for the 84 papers included in this analysis was 0.9, indicating that most publications contained too many flaws. It is not surprising that MP have been noted in shellfish guts globally. What is surprising is the extremely low level of particles routinely recorded (see Table 1 and references therein). The presence of MP in molluscs has been shown repeatedly, with little regard for quality assurance and control measures. The inconsistencies across studies and lack of proper sampling design have inundated the literature with incomparable studies and inappropriate claims. Common mistakes in field studies from collection through digestion and MP characterization are discussed and identified in 128 studies. Suggestions are made to improve field studies at every stage. The data to date clearly demonstrate extremely low numbers (<10 per individual) of MP in filter-feeding bivalve molluscs globally. There are no data demonstrating presence of MP in these molluscs is a serious risk to human health, and few data to demonstrate negative impacts on the shellfish at environmentally relevant concentrations. Many of the studies on suspension-feeding bivalve molluscs and other invertebrates are weak or fatally flawed. There is a recurring presence in the published literature of misunderstanding of the feeding processes, capabilities for particle selection and rejection, and species-specific differences that all lead to misinformation, misinterpretation, and incorrect assumptions regarding potential impacts. There are major shortcomings to many laboratory studies that examined uptake and accumulation of MP by bivalves and their subsequent effects. The shortcomings have led to a seriously flawed literature on purported interactions and impacts of MP on these animals. If potential investigators do not possess the necessary knowledge and skills to carry out the study, they should engage a collaborator that has the requisite expertise. Bivalves and other particle-feeding molluscs are complex living organisms with extraordinary capabilities for the control of selective capture, ingestion, and egestion of particulate material. They should be recognized and treated as such in any attempt to describe impacts of stressors, including different particle types, on their feeding and ability to accumulate materials. Any future experimental studies need to be focused carefully, based upon clear questions, use standardized analytical procedures, demonstrate a knowledge of the animals being studied, and an understanding of the literature extant. The hype needs to be curtailed and scientists should not imply impacts or potential impacts when there are no data to support the suppositions at environmentally relevant concentrations of MP. The case is further strengthened to stop advocating for the use of bivalve molluscs as reliable indicators of MP in the environment. Recommendations are offered for future efforts including harmonization of methodologies. Finally, a plea is made for editors of scientific journals to make a stronger effort to engage qualified peer-reviewers and stop the flow of poorly done studies and superficial reviews that do nothing more than confuse the literature and reinforce inadequate studies and prior reviews. This review is presented from the viewpoint and consideration of experts in shellfish physiology, and represents the opinions of, and assessments made by, the authors.

Keywords:

• Microplastics
• molluscs
• peer review
• bioindicators
• methodology

Acknowledgments

Dr. Jay Parsons of the Editorial Board handled the review process and the authors thank him and four anonymous reviewers for their input. Drs. Stephan Bullard, Joth Davis, Paul Dayton, Simone Duerr, Kay Ho, John Icely, Bill Lucey, Alice Newton, Robert Rheault, Brian Rothschild, and Paul Zajicek provided insightful comments on earlier versions of the manuscript.

Additional information

Funding

This work was partially supported by grants from the National Oceanic and Atmospheric Administration, Marine Debris Program NA17NOS9990121 (J.E.W. and S.E.S.); Long Island Sound Study Award # 1157712/2/86473; Connecticut Sea Grant (R/A-48).