# Marine and freshwater mussels as biomonitors for microplastic concentrations: a comparative laboratory study

Adèle Wolinski, Miléna Ferret, Basile Bergeron, Loïc Tettling, Edouard

Lavergne, Audrey M. Pruski, Isabelle Calvès, Anne-Leïla Meistertzheim,
Franck Lartaud

► To cite this version:

Adèle Wolinski, Miléna Ferret, Basile Bergeron, Loïc Tettling, Edouard Lavergne, et al.. Marine and freshwater mussels as biomonitors for microplastic concentrations: a comparative laboratory study. Aquatic Toxicology, 2025, 291, pp.107659. 10.1016/j.aquatox.2025.107659. hal-05387003v2

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# Marine and freshwater mussels as biomonitors for microplastic concentrations: A comparative laboratory study

Adèle Wolinski<sup>a,b</sup>, Miléna Ferret<sup>b</sup>, Basile Bergeron<sup>b</sup>, Loïc Tettling<sup>b</sup>, Edouard Lavergne<sup>b</sup>,
Audrey M. Pruski<sup>a</sup>, Isabelle Calvès<sup>b</sup>, Anne-Leïla Meistertzheim<sup>b</sup>, Franck Lartaud<sup>a,*</sup>

## ARTICLE INFO

**Keywords:**

Mytilus galloprovincialis

Dreissena spp.

Uptake

Depuration

Bioindicators

Microplastic pollution

## ABSTRACT

Microplastics are pervasive in both freshwater and marine waters, posing potential hazards to a wide range of species. Evaluating environmental microplastic pollution is crucial for ecological risk assessment. However, current monitoring methods, such as sampling nets, are inefficient for quantifying small microplastics (< 25 µm) and non-buoyant particles, leading to potential underestimation of pollution levels. Biomonitors, like suspension-feeding organisms, can serve as complementary tools. This study takes a first step in evaluating bivalves as biomonitors by assessing whether microplastic uptake in their tissues correlates with environmental concentrations in both marine and freshwater conditions. Two mussel models, the marine *Mytilus galloprovincialis* and the freshwater *Dreissena* spp., were exposed to varying concentrations of microplastics (from 0 to 2000 MPs.L⁻¹) over 48 h. Both marine and freshwater mussels followed a linear model for MP uptake. However, an exponential model appeared more suitable for *M. galloprovincialis* whereas a Gaussian model better described the uptake pattern in *Dreissena* spp., suggesting the presence of a threshold in MP capture for the latter species. Microplastics primarily accumulated in the digestive gland compared to other tissues (i.e., byssus, gills, mantle, and others). After 48 h of depuration, marine mussels exhibited a high microplastic depuration rate (from 88 to 97%), while freshwater mussels showed moderate depuration ability (from 0 to 71%). These results support *M. galloprovincialis* as an effective biomonitor for marine microplastic pollution. In freshwaters, the non-linear accumulation of microplastics by *Dreissena* spp. limits their suitability for precise pollution assessment, but may help set pollution alert levels based on MP content and sub-lethal effects. This study contributes to addressing the challenge of accurate MP quantification in aquatic environments by highlighting the potential of bioindicators in complementing traditional methods.

## 1. Introduction

Plastic is a material widely used in industries such as agriculture, construction, and packaging (Geyer et al., 2017). Since its market launch in the 1950s, plastic production has surged, reaching 400 million tons in 2022 (Plastics Europe 2024). Plastic popularity stems from its properties, including light-weight, strength, affordability, and durability (Barnes et al. 2009; Thompson et al. 2009). This latter feature contradicts with short-term usages of plastic, particularly in packaging, which accounts for 31 % of global plastic applications (OECD 2022). As a result, large amounts of persistent waste are generated and, due to inadequate collection and recycling systems (Sardon and Dove 2018;

Diggle and Walker 2022), a significant portion ends up in the environment. Physical and biological processes lead to the fragmentation of large plastic items, known as “macroplastics” (> 25 mm), into smaller particles called secondary “microplastics” (MPs, < 5 mm) (Andrady 2011; Van Cauwenberghe et al. 2015). In addition, primary MPs (i.e., manufactured purposely as MPs (Coyle et al. 2020) for applications in industry or cosmetics) enter the environment through transport leaks, road runoff, wastewater discharge, and wind dispersal (Boucher and Friot 2017). Both types of MPs are now widespread in marine and freshwater environments (Eerkes-Medrano et al. 2015; Pabortsava et Lampitt 2020).

The small size of MPs, similar to phytoplankton (Bermúdez and

<footnote><sup>a</sup> Sorbonne Université, CNRS, Laboratoire d'Écogéochimie des Environnements Benthiques (LECOB), UMR 8222, Observatoire Océanologique de Banyuls, Banyuls-sur-Mer F-66650, France</footnote>

<footnote><sup>b</sup> SAS Plastic At Sea, 17 avenue Pierre Fabre, Banyuls-sur-Mer 66650, France</footnote>

<footnote>* Corresponding author.</footnote>

<footnote>E-mail address: lartaud@obs-banyuls.fr (F. Lartaud).</footnote>
Swarzenski 2021), makes them bioavailable and easily ingested by a wide range of aquatic organisms, from zooplankton, to molluscs, fishes, and large mammals (Cole et al. 2013; Egbeocha et al. 2018). Accumulation of MPs in biota is of particular concern due to potential ecological and sanitary risks (Leistenschneider et al. 2023; Van Cauwenberghe and Janssen 2014). Indeed, several studies have documented the accumulation of MPs in commercially important seafood species such as mussels, clams, and oysters (Jiana et al., 2018; Cho et al. 2019), raising concerns that MPs may enter the human food web and impact seafood security and fishery sustainability in the future (Smith et al. 2018; De-la-Torre 2020; Cunningham et al. 2022; Joyce et al. 2023). This has heightened interest among various stakeholders, including governments, environmental Non-Governmental Organisations (NGOs), the media, and citizens in monitoring MP pollution (Fossi et al. 2018).

However, quantifying MPs in aquatic environments remains challenging. The most common method, Manta net sampling, is limited to buoyant particles larger than 300–350 µm (Pasquier et al. 2022). Smaller mesh sizes are rarely used in research, and none exist below 25 µm (Ter Halle et al. 2017; Pasquier et al. 2022), leading to a lack of data on the abundance and distribution of small MPs (< 25 µm) within the water column (Song et al. 2015; Yu et al. 2025). Moreover, the efficiency and reliability of net-based MP sampling can be affected by meteorological and hydrodynamic constraints, as well as limited replication (Pasquier et al. 2022). To address these limitations, complementary monitoring tools are needed. For instance, the United Nations Environment Program (UNEP) has highlighted the potential of bioindicator species (i.e., organisms providing information on the quality of the environment (Beeby 2001)) to monitor MPs (Garcia-Garin et al. 2019). By assessing MP bioavailability, bioaccumulation, and potential toxic effects, bioindicators offer a more comprehensive approach to evaluate MP pollution and its ecological risks.

Filter-feeding bivalves, and particularly mussels, are strong candidates for bioindication (Li et al. 2019; Pastorino et al. 2021) due to their abundance, sedentary lifestyle, ease of identification and sampling (Bonanno and Orlando-Bonaca 2018). Their wide distribution in both marine and freshwater habitats also makes them valuable for bio-monitoring along land-sea continuums, which are relevant frameworks for studying the sources and fate of MP pollution in aquatic environments (Rowenczyk et al. 2022). As suspension-feeders, mussels filter large volumes of water (Riisgård et al. 2014; Kazour et Amara 2020) to feed on suspended particles (Harris and Carrington 2020), capturing a broad range of natural and synthetic particles present in the environment (Zhao et al. 2018).

MPs have been detected in marine mussels from over twenty countries (Li et al. 2021), with *in situ* studies revealing a correlation between abundance and characteristics of MPs in water and those found in marine mussels (Qu et al. 2018; Li et al. 2019; 2021). This supports their use as biomonitors (i.e., bioindicators holding quantitative information on the health of the ecosystem (Beeby 2001)), offering a means to assess small MPs not collected by nets. MPs have also been found in freshwater mussels of the genus *Dreissena* (Pastorino et al. 2021), but individual variation in MP burden often matches or exceeds variation between sites (Hoellein et al. 2021). Therefore, controlled laboratory experiments are needed to better characterise MP uptake and depuration abilities of marine and freshwater mussels, ultimately refining their application as quantitative (MP abundance) and qualitative (MP types) monitoring tools for MP pollution in aquatic environments (Bonanno and Orlando-Bonaca 2018).

This study evaluates whether marine *Mytilus galloprovincialis* and freshwater *Dreissena* spp. mussels could be used as MP biomonitors by (i) validating the MP uptake by both mussel models; (ii) analysing the relationship between MP concentration in the water and uptake by mussels; (iii) investigating the MP distribution within mussel tissues; and (iv) quantifying the depuration ability of MPs in mussels. To focus on realistic concentrations of MP in the environment, we used various concentrations ranging from 0 to 2000 MP.L⁻¹ as such high values have

been reported in heavily polluted areas, both in coastal marine and freshwater environments (Li et al., 2020; Buhhalko et al., 2025). Due to differences in filtration rates between the two species, we expect marine mussels to capture more microplastics than freshwater mussels, but with a lower potential for particle retention due to higher fecal pellets egestion rates.

## 2. Material and methods

### 2.1. Mussel sampling and acclimation

About 200 mussels *Mytilus galloprovincialis* mussels (shell length of 6.4 ± 0.5 cm) were collected by divers in March 2023 at the SOLA buoy (42°29'300 N – 03°08'700 E) in the bay of Banyuls-sur-Mer (Gulf of Lion, Northwestern Mediterranean Sea, France) and placed in a net for their transportation to the laboratory across the street (~15 min after collection). Marine mussels were then separated from each other and cleaned with a brush to remove epiphytes before being placed in a 180 L aquarium filled with aerated 25 µm-filtered seawater pumped at 14 m depth in the bay of Banyuls-sur-Mer (salinity of 38 g.L⁻¹), and maintained at 18 °C.

Approximately 1500 dreissenid mussels (shell length of 2.5 ± 0.4 cm) were collected in September 2023 at 12 m depth by a professional fisherman at the Bourget Lake (45°43'46.842" N – 5°52'10.484" E, Savoie, France). Both *Dreissena polymorpha* and *Dreissena bugensis* inhabit this sampling area. Although most of the mussels collected were *D. bugensis*, we chose to refer to them as *Dreissena* spp. since distinguishing between the two species can be challenging. Dreissenids were placed in a bucket filled with *in situ* water and equipped with a bubbler for their transportation to the laboratory (lasting ~6 h), where they have been separated from each other and cleaned. The freshwater mussels were then placed in a 100 L aquarium filled with aerated water from the Bourget Lake for the first day of acclimation, and maintained at 18 °C. On the second day, 1/3 of the water was replaced with a 50:50 (v/v) mixture of filtered tap water and deionised water (Magni et al. 2018; Louis et al. 2021). This operation was repeated over the following two days to gradually replace all of the site water.

For both mussel models, acclimation lasted 7 days, and both the acclimation and the experiment were conducted in a room set at 18 °C with a 12:12 photoperiod, with lighting from 7 AM to 7 PM. The physicochemical parameters of the water (NO₂, NO₃, NH₄, pH) were monitored twice a week with colorimetric tests (ProAquaTest, JBL Gmbh & Co. KG, Germany) and the water temperature was checked daily. Marine mussels *M. galloprovincialis* were fed daily with a mixture of *Tetraselmis* spp. and *Isochrysis* spp. (10⁷ cells.mL⁻¹, produced by the Aquariological Service of the Oceanological Observatory of Banyuls-sur-Mer), while freshwater *Dreissena* spp. mussels were fed with a suspension of *Chlorella* spp. (20.10⁷ cells.mL⁻¹, provided by Greensea, France). The selected diets are recognized as being suitable and specific to these species for their breeding in aquaria, particularly for toxicological studies including microplastics (Zhong et al., 2013; Pizzurro et al., 2023).

### 2.2. Microplastic preparation

The MPs used for this experiment were fluorescent polyethylene (PE) microspheres, 10 – 20 µm in diameter (particle density: 1.00±0.01 g.cm⁻³ specifically designed for neutrally buoyancy in aqueous solutions, fluorescence emission peak of 525 nm when excited at 485 nm; Figure S1) manufactured for scientific use and purchased as a dry powder from Cospheric (USA). PE was chosen because it is the most abundant plastic in the world, used to manufacture plastic bags and bottles (Garcia-Garin et al. 2019), and one of the most commonly found polymer in aquatic environments along the land-sea continuum (Philip et al. 2024) and in mussel tissues (Hermabessiere et al. 2019; Expósito et al. 2022; Fraissinet et al. 2024). This size of MPs was selected based on
the size of particles that mussels typically feed on (Harris and Carrington 2020) while being too small to be collected by classical quantification methods (i.e., nets). To facilitate the preparation for MP exposure in the aquaria, a MP stock solution was prepared in 70 % ethanol in a glass tube to achieve a final concentration of 100 000 MPs.mL⁻¹. Ethanol was used to ensure thorough dispersion of the microbeads in the solution, as recommended in the review by Karami (2017). Before each MP exposure, the suspension was homogenized by a vigorous shaking of the bottle. At each water change, up to 1 mL of the 70 % EtOH suspension were delivered to the 50 L aquaria to obtain the desired final MP concentrations, resulting in a final EtOH concentration of 14 ppm. The same volume of 1 mL of MP free 70 % EtOH was also added to the control tank at each water change to consider the potential effect of EtOH. Concentration of the stock solution was verified via flow cytometry and microscopy. Just before MP introduction, the suspension was homogenised by vortexing the stock solution for a few seconds with a visual confirmation of no particle aggregation on the surface.

## 2.3. Experimental design

Marine and freshwater mussels were placed in PlastiCell® structures (patent BT8167PC00, Plastic At Sea Company, France, see Figure S2 and Text S1 for more details) to ensure a great bioaccessibility of MPs to the organisms. They were placed in pairs in each PlastiCell®, with 8 PlastiCell® per structure (n = 16) and one structure for each exposure concentration. According to the literature, MP exposure experiments may range from 100 to 1000 MPs.L⁻¹ to reflect realistic conditions for marine environments (Baroja et al. 2021; Leistenschneider et al. 2023), while MP concentrations in freshwater environments range from 0.016 to 2867 MPs.L⁻¹ (Li et al. 2020). Therefore, for *M. galloprovincialis*, a gradient of 7 concentrations of MPs was used: 0 (as control), 100, 200, 500, 1000, 1500 and 2000 MPs.L⁻¹. As *Dreissena* spp. Mussels are smaller and thus more likely to be sensitive to lowest variation in MP concentrations, 3 concentrations were added to the previous gradient: 50, 150 and 350 MPs.L⁻¹. After 48 h of exposure, one mussel from each PlastiCell® in each structure was sacrificed and dissected (referred to as “exposed mussels”, *n* = 8 per structure). The 48-h exposure time was selected based on the findings of Wei et al. (2021), who demonstrated that the highest MP uptake in *M. galloprovincialis* was achieved at this time point.

The 8 remaining mussels in each PlastiCells® structures were transferred into small glass aquaria – one per exposure concentration – to avoid confusion. They were then placed in a 120 L aquarium filled with clean water for an additional 48 h of depuration. The water in the aquarium was continuously pumped to pass through two types of filtration wadding (Symec and Symec XL, JBL Gmbh & Co. KG) to capture the MPs depurated by mussels and avoid as much as possible self-contamination (see Figure S3 and Text S2 for more details of the depuration system). After 48 h of depuration in clean water, the mussels

## 2.4. Dissection and sample preparation

Marine and freshwater mussels were dissected either immediately after the 48-h exposure (exposed mussels) or after an additional 48-h depuration period (depurated mussels). For *M. galloprovincialis*, 4 mussels of each of the exposed and depurated groups at each exposure concentration were dissected, with the main tissues separated (i.e., byssus, gills, mantle, digestive gland, and a pooled sample of other tissues, including gonads, labial palps, muscles, viscera and the foot). The remaining 4 mussels from each group were dissected whole, with the flesh separated from the shells. For dreissenids, all mussels were dissected whole due to their small size. Metal scalpels, scissors and tweezers were used for the dissection. After being opened, the tissues were rinsed with seawater for marine mussels and distilled water for dreissenids to remove any potential MPs from the mantle cavity. All tools were carefully washed with 70 % ethanol and ultrapure water and wiped between samples. Each organ or whole mussel was placed in a 25 mL glass tube, freeze-dried for 24 h, and then weighted on a microscale (Mettler-Toledo, France) to determine its dry weight (DW).

## 2.5. Digestion, filtration and quantification of microplastics

In each tube containing freeze-dried tissues or whole mussels, 20 mL of 10 % potassium hydroxide solution (10 % KOH, Sigma-Aldrich, USA) were added. Samples were digested in an oven at 60 °C with orbital shaking for 48 h for marine mussels and 24 h for freshwater mussels, due to their smaller size and lower tissue mass. The digested samples were then filtered onto 1.2 µm fiberglass filters (GF/C diameter 47 mm from Whatman® Sigma-Aldrich) using a glass filter unit coupled to a vacuum pump. For each sample, the tube and the filtration unit were abundantly rinsed twice with ultrapure water and 70 % ethanol to ensure that all MPs were collected on the filter. The filtration unit was also carefully rinsed between samples to avoid cross-contamination. The filters were then placed in small Petri dishes and left to dry few hours at room temperature. Fluorescent MPs collected on the filters were counted manually using an epifluorescence microscope (BX-UCB, Olympus, Japan) with FITC filter (excitation peak = 490 nm, emission peak = 525 nm).

## 2.6. Data and statistical analysis

For marine mussels, to determine the total number of MPs per individual, the number of MPs from each tissue, except for the byssus, was summed. To calculate the number of MPs per mg of DW of marine and freshwater mussels, the total number of MPs for each individual was divided by its weight after freeze-drying. To estimate the ability of MP depuration by marine and freshwater mussels, MP depuration rates were calculated for each concentration exposure following the formula:

(Median number of MPs in exposed mussels – Median number of MPs in depurated mussels) * 100

Median number of MPs in exposed mussels

referred to as “depurated mussels” were sacrificed and dissected.

For both exposure and depuration periods, the water used to fill the aquaria was filtered through 1–3 µm pore-size filters using aquarium-grade filter columns (JBL, Germany), on seawater pumped at 14 m depth in the bay of Banyuls-sur-Mer for *M. galloprovincialis*, and a 50:50 (v/v) mixture of filtered tap water and deionized water for *Dreissena* mussels. There was no mortality during the 48-h exposure or depuration periods.

Statistical analyses were performed using R v4.3.1 (R Core Team, 2025) with a significance threshold of *p* < 0.05. To compare the abundance of MPs in whole mussels or in separated tissues across the different exposure concentrations, a non-parametric analysis (Kruskal–Wallis), followed by Dunn post-hoc test for pair comparisons were done as the data did not meet normality (Shapiro-Wilk test) or homoscedasticity (Bartlett test) assumptions. Wilcoxon tests were performed to compare the abundance of MPs between exposed and depurated mussels
<figure><img src="image_2.png" /><figcaption>**Fig. 1.** Number of MPs found in (A) mussels *M. galloprovincialis* and in (B) *Dreissena* spp. depending on the exposure concentration, for exposed (black) and depurated (white) mussels (n = 8 for each exposure concentration). Boxplots correspond to the median ± lower and upper quartiles, red diamonds represent the averages, and black dots represent the outliers. Uppercases and lowercases show significant differences among exposure concentrations in exposed and depurated mussels, respectively (Kruskal-Wallis test followed by Dunn post-hoc test, *p* < 0.05). Models of the relationship between the median number of MPs found in mussels (C) *M. galloprovincialis* and (D) *Dreissena* spp. and the exposure concentration. Grey dots represent individual data and black dots represent the median for each exposure concentration. Blue, red, and yellow lines represent the linear, the exponential, and the Gaussian models, respectively.</figcaption></figure>

<figure><img src="image_3.png" /></figure>

for each exposure concentration. The relationship between the median number of MPs per individual or per separated tissue and the exposure concentration was modelled, with coefficients of determination (R²) provided for the most appropriated model. The correlation between MP depuration rates and exposure concentrations was tested using a Spearman test.

# 3. Results

## 3.1. Microplastic uptake

The median number of MPs found in marine mussels *M. galloprovincialis* exposed to 100 to 2000 MPs.L⁻¹ varied from 96 to 1056 MPs.individual⁻¹ (Fig. 1A) and from 0.1 to 1.3 MPs.mg⁻¹ of DW (Table S1). Although mussels exposed to the higher concentration of particles exhibit a higher range of MP uptake, the relationship between the median abundance of MPs in mussels and the water concentration can be assessed by a positive linear correlation (R² of 0.91, *p* < 0.05) or an exponential model (R² of 0.99, *p* < 0.05) (Fig. 1C, Table S2).

Likewise, the number of MPs in freshwater mussels after 48 h of exposure increased with increasing concentrations (Fig. 1B). The median abundance of MPs in *Dreissena* spp. Mussels exposed from 50 to 2000 MPs.L⁻¹ varied from 2 to 109 MPs.individual⁻¹ and from 0.0 to 3.2 MPs.mg⁻¹ of DW (Table S3). The relationship between MP uptake by freshwater mussels and their exposure conditions was described by a

<caption>**Table 1**</caption>

MP depuration rates after 48 h of depuration in clean water for mussels *M. galloprovincialis* and *Dreissena* spp. ‘n.a.’ corresponds to the three concentrations to which marine mussels were not exposed.

<table><thead><tr><th rowspan="2">Exposure concentration (MPs.L<sup>-1</sup>)</th><th colspan="2">MP depuration rates (%)</th></tr><tr><th><i>M. galloprovincialis</i></th><th><i>Dreissena</i> spp.</th></tr></thead><tbody><tr><td>50</td><td>n.a.</td><td>33</td></tr><tr><td>100</td><td>93</td><td>71</td></tr><tr><td>150</td><td>n.a.</td><td>0</td></tr><tr><td>200</td><td>89</td><td>50</td></tr><tr><td>350</td><td>n.a.</td><td>65</td></tr><tr><td>500</td><td>93</td><td>46</td></tr><tr><td>1000</td><td>88</td><td>64</td></tr><tr><td>1500</td><td>92</td><td>52</td></tr><tr><td>2000</td><td>97</td><td>50</td></tr><tr><td>All concentrations combined</td><td>92 ± 3</td><td>48 ± 21</td></tr></tbody></table>

linear regression (R² of 0.85, *p* < 0.05) and a Gaussian model (R² of 0.99, *p* < 0.05) (Fig. 1D, Table S4). The Gaussian model appeared more biologically realistic and robust, and gives a maximum of 109 MPs.individual⁻¹ (corresponding to 3.2 MPs.mg⁻¹ of DW), reached at the exposure concentration of 1537 MPs.L⁻¹.
## 3.2. Microplastic depuration rates

After 48 h of depuration in clean seawater, the median abundance of MPs remaining in marine mussels previously exposed to all concentrations varied from 7 to 27 MPs.individual⁻¹ (Fig. 1A) and from 0.0 to 0.1 MPs.mg⁻¹ of DW (Table S1). The MP depuration rates of *M. galloprovincialis* ranged from 88 to 97 %, with an average of 92 ± 3 % all concentrations combined (Table 1). No correlation was observed between the depuration ability of MPs and the exposure concentration (Spearman test, *p* > 0.05).

The median abundance of MPs found in freshwater mussels after 48 h of depuration varied from 1 to 53 MPs.individual⁻¹ (Fig. 1B) and 0.0 to 1.6 MPs.mg⁻¹ of DW (Table S3). Unlike marine mussels, dreissenids exhibited moderate and highly variable MP depuration rates across the different exposure concentrations, averaging 48 ± 21 % and ranging from 33 to 71 %, except for the exposure concentration of 150 MPs.L⁻¹, where the depuration rate was zero. Still, no correlation was observed between the depuration ability of MPs and the exposure concentration (Spearman test, *p* > 0.05).

## 3.3. Microplastic distribution within the tissues of marine mussels

After 48 h of exposure, the distribution of MPs varied across the different tissues of marine mussels (Fig. 2A, Table S5). For individuals exposed to the first five concentrations, ranging from 100 to 1500 MPs. L⁻¹, the partitioning of MPs within tissues followed a consistent pattern: digestive glandª > other tissuesab > byssusabc > mantleb ≈ gillsc (superscript letters show significant differences for all concentrations combined, Kruskal-Wallis test followed by Dunn post-hoc test, *p* < 0.05). Between 45 and 82 % of the total MP uptake were found into the digestive gland. In contrast, marine mussels exposed to the highest concentration (2000 MPs.L⁻¹) displayed a more balanced distribution of

<figure><img src="image_4.png" /><figcaption>**Fig. 2.** Number of MPs in the different tissues depending on the exposure concentration in mussels *M. galloprovincialis* after (A) 48 h of exposure and (B) 48 h of depuration (n = 4 for each exposure concentration). Boxplots correspond to the median ± lower and upper quartiles, yellow diamonds represent the averages, and black dots represent the outliers. Lowercases show significant differences among exposure concentrations for each tissue (Kruskal-Wallis test followed by Dunn post-hoc test, *p* < 0.05).</figcaption></figure>

MPs between the digestive gland and other tissues (gonads, palps, muscles, and the foot), with 41 and 46 % of the total MP uptake, respectively (Fig. 2).

Positive correlations between the median abundance of MPs in water and in the separated tissues of marine mussels were also observed (Fig. 3). A linear correlation was found for all types of tissues but fits better for the gills (R² of 0.96) while exponential models were more suitable for byssus and mantle (R² from 0.94 to 0.97). For the digestive gland, a sigmoidal model seemed more appropriate (R² of 0.97) whereas an exponential one was convenient for the other tissues (R² of 0.99).

After depuration, the remaining MPs in marine mussel tissues were significantly reduced compared to the levels observed after exposure (Wilcoxon test, *p* < 0.05), and more evenly distributed between the different types of tissues (Fig. 2B, Table S5). Byssus contained the highest abundance of residual MPs, with a median ranging from 3 to 28 MPs.individual⁻¹ and from 0.1 to 1.1 MPs.mg⁻¹ of DW (Table S5).

The tissues with the greatest MP depuration rates were the digestive gland and the other tissues, ranging from 87 to 99 % for the digestive gland and from 40 to 99 % for the other tissues, depending on the exposure concentration (Table 2). In contrast, MPs were the most persistent in the byssus, with an average MP depuration rate of 45 ± 34 %. No correlation was found between the ability of the tissue to depurate MPs and the exposure concentration, except for the byssus (Spearman test, *p* < 0.05).

# 4. Discussion

## 4.1. Marine mussels monitor efficiently microplastics in seawater

Our study clearly demonstrated that the uptake of 10 – 20 µm PE microspheres by marine *M. galloprovincialis* mussels over 48 h depends on their concentration in seawater. While an exponential model better described the relationship, it is strongly influenced by scattered values at high exposure concentrations (1500 and 2000 MPs.L⁻¹). This high inter-individual variability is frequent in pollutant accumulation in mussels (Mubiana et al. 2006; Benito et al. 2023). The positive linear correlation, even at the highest exposure level (2000 MPs.L⁻¹), appears suitable and suggests that marine mussels could effectively monitor a wide range of MP concentrations in ambient seawater. Woods et al. (2018) measured maximum MP uptake rates by *M. edulis* exposed to polyethylene terephthalate (PET) microfibers at 13 000 MPs.L⁻¹, approximately seven times higher than our highest tested concentration. This further indicates that marine mussels could be valuable for monitoring high levels of MP pollution at sea.

A positive and quantitative relationship between MPs in marine mussels and their surrounding waters has previously been documented in the literature in both laboratory (Setälä et al. 2016; Qu et al. 2018) and field studies (Jiana et al., 2016; Qu et al. 2018). For instance, we determined a strong linear correlation with the results obtained by Setälä et al. (2016) after a 24-h exposure of *M. trossulus* to 3 concentrations (5, 50 and 250 MPs.mL⁻¹) of 10 µm polystyrene (PS) microbeads (R² of 0.99) (Fig. 4). The slope of the regression line is 2.6, thus 6 times greater than the one we have obtained, probably due to the concentrations applied which are much higher than in our experiment. Age of mussels, and thus their filtration rates, between the two experiments can also explain the differences in MP uptake as mussels from our study are expected younger compared to the one from Setälä et al. (2016), based on the known age model of these species (Millstein and O'Clair, 2001; Andrisoa et al., 2019). Likewise, in the field study of Qu et al. (2018), linear relationship between MP concentration in marine *M. edulis* mussels and site surrounding water was found (R² of 0.75 based on MPs per gram of mussels, and 0.44 based on MPs per individual). The regression line showed a slope of 1.1 (Fig. 4), which is closer to the slope observed in our study. In their study, Qu et al. (2018) report that the values measured in mussels exposed to MP under laboratory conditions are lower compared to analyses done on samples from the field, likely
<figure><img src="image_5.png" /><figcaption>**Fig. 3.** Models of the relationships between the median number of MPs found in (A) the byssus, (B) the gills, (C) the mantle, (D) the digestive gland and (E) the other tissues of mussels *M. galloprovincialis* and the exposure concentration (MPs.L⁻¹). Grey dots represent individual data and black dots represent the median for each exposure concentration. Blue, red and green lines represent the linear, the exponential and the sigmoidal regressions, respectively.</figcaption></figure>

<caption>**Table 2**</caption>

MP depuration rates after 48 h of depuration in each tissue for mussels *M. galloprovincialis*.

<table><thead><tr><th rowspan="2">Exposure concentration (MPs. L<sup>-1</sup>)</th><th colspan="5">MP depuration rates (%)</th></tr><tr><th>Byssus</th><th>Gills</th><th>Mantle</th><th>Digestive gland</th><th>Other tissues</th></tr></thead><tbody><tr><td>100</td><td>0</td><td>100</td><td>86</td><td>88</td><td>91</td></tr><tr><td>200</td><td>17</td><td>0</td><td>80</td><td>91</td><td>74</td></tr><tr><td>500</td><td>30</td><td>81</td><td>53</td><td>91</td><td>58</td></tr><tr><td>1000</td><td>64</td><td>71</td><td>44</td><td>87</td><td>40</td></tr><tr><td>1500</td><td>81</td><td>67</td><td>58</td><td>99</td><td>89</td></tr><tr><td>2000</td><td>80</td><td>79</td><td>83</td><td>99</td><td>99</td></tr><tr><td>All concentrations combined</td><td>45 ± 34</td><td>66 ± 34</td><td>67 ± 18</td><td>93 ± 5</td><td>75 ± 23</td></tr></tbody></table>

related to the diversity of MP in the environment, in term of shape, size, colors, composition and additives, and/or a longer exposure period at sea compared to aquaria conditions. Thus the values observed in our study could underestimate the uptake rate in natural environments for

<figure><img src="image_6.png" /><figcaption>**Fig. 4.** Linear model between the median number of MPs found in mussels *M. galloprovincialis* and the exposure concentration (blue, with the blue shaded area representing the 95 % confidence interval), along with linear regressions based on data from *M. trossulus* in Setälä et al. 2016 (purple) and *M. edulis* in Qu et al. 2018 (pink).</figcaption></figure>
### *M. galloprovincialis*

Our study focused exclusively on the uptake of a single type of MPs. However, previous studies have demonstrated that the dominant morphotype and polymeric composition of MPs found in mussels tend to align with those present in their surrounding environment (Qu et al. 2018; Railo et al. 2018). This correspondence can provide valuable insights into pollution sources, such as microbeads from plastic industries or fibres from wastewater treatment plants (Ramasamy et al. 2022). This suggests that MPs in marine mussel tissues can accurately reflect both the concentration and type of MP pollution at sea, supporting the use of marine *Mytilus* mussels as biomonitors. Although our results are valid only for a 48-h exposure and should be verified for longer durations, this approach can be useful for assessing recent contamination events, such as industrial leaks, accidental discharges, or human activities with an environmental footprint (e.g., festivals, beach cleanups).

Our study displays that MPs are not evenly distributed between the different tissues of marine mussels, following a pattern: digestive gland > other tissues > byssus > mantle ≈ gills, which is consistent with previous research (Wei et al. 2021; Calmão et al. 2023). In bivalves, two routes of MP uptake have been identified: the adherence and the ingestion (Kolandhasamy et al. 2018; Sendra et al. 2021). In our study, adherence can explain the presence of MPs in gills, mantle, and other tissues, but ingestion appears as the primary pathway, as most MPs are found in the digestive gland across all exposure concentrations. This organ has already been shown to be the major target for small MPs and nanoplastics (NPs, < 1 µm) (Gaspar et al. 2018; Sendra et al. 2020; Huffman Ringwood 2021). However, we suggest a threshold here, as at our highest exposure concentration (i.e., 2000 MPs.L⁻¹), MPs were evenly distributed between the digestive gland and the other tissues, possibly due to MP transfer via the circulatory system (Browne et al. 2008), or reduced water flow when the digestive gland is saturated (Riisgård et al. 2011), allowing MPs to adhere better to other tissues. High MP levels were also detected in byssal threads, which may result from passive adhesion of particles present in the water, incorporation from the mantle cavity (Li et al., 2019), or active transfer from soft tissues, as it is the case for heavy metal elimination (Szefer et al. 2006).

After a 48-h exposure followed by 48 h in clean seawater, marine mussels exhibited high MP depuration rates (92 ± 3 %), regardless of exposure concentration. This aligns with previous studies demonstrating that marine mussels rapidly expel most MPs (Woods et al. 2018; Kolandhasamy et al. 2018; Birnstiel et al. 2019; Fernández et Albentosa 2019a). This great ability to depurate quickly the MPs indicates that the MP abundance measured in tissues of marine mussels at a given time represents well the current MP pollution of the water. This point should however be checked by extended exposure durations to confirm the constancy of their uptake and depuration rates over time.

Nevertheless, about 10 % of MPs remained in marine mussels after a 48-h depuration. Studies suggest that some MPs can persist for a long period (Browne et al. 2008; Kinjo et al. 2019), even after a brief exposure (e.g., 3 h for the two studies mentioned above). MP retention time in mussel tissues varies depending on particle shape and type (Kinjo et al. 2019). For instance, Kolandhasamy et al. (2018) reported that only 30–40 % of microfibers were depurated by M. edulis after a 48-h exposure at 2000 particles.L⁻¹ followed by a 48-h depuration. Moreover, small particles tend to be retained longer (Van Cauwenberghe et al. 2015; Fernández and Albentosa 2019a; 2019b; Wang et al. 2021). Therefore, further research is needed to develop a reliable biomonitor that accounts for the full diversity of MPs.

## 4.2. Limits of using freshwater mussels as a biomonitor of microplastics

The freshwater *Dreissena* spp. mussels exhibited a higher MP uptake at the highest exposure levels. Likewise, Pedersen et al. (2020) found a positive relationship between MP concentration in water and in quagga mussels. In our study, a Gaussian model better described the MP uptake in dreissenids than a linear model. Similarly, Weber et al. (2021) found

that MP body burden in *D. polymorpha* did not increase linearly with exposure.

The Gaussian model suggests a weak MP uptake at low environmental concentrations (from 50 to 500 MPs.L⁻¹) which does not accurately reflect variations in the surrounding freshwater pollution levels. This aligns with *in situ* observations by Hoellein et al. (2021), who reported low MP levels in *Dreissena* spp. despite variations in water MP concentrations among sites. However, between 500 and 1500 MPs.L⁻¹, the MP uptake appears to be linear. The decline in MP content above 1500 MPs.L⁻¹ may indicate that the tolerance threshold of dreissenids for MPs was exceeded, potentially impacting their health and/or behaviour, and thereby reducing their MP uptake. Adverse effects have already been demonstrated on dreissenids under high MP concentrations (e.g., changes in antioxidant capacity (Magni et al. 2018; Weber et al. 2020; Binelli et al. 2020), modulation of proteins (Magni et al. 2019; Brehm et al. 2022), effects on clearance rates (Weber et al. 2021)). Bivalves exhibit classically reduced clearance rate and adverse effects on physiological performance when exposed to high concentration of MP (Huaxin et al., 2020). A recent study using similar types of MP showed that *Dreissena* exposed to 2000 MP.L⁻¹ for 15 days had low energy intake and high mortality, whereas they appeared unaffected at 200 MP.L⁻¹ (Wolinski et al., 2025). This change in health status might explain the decrease in MP uptake at higher exposure levels and the maximum of MP capture observed at 1537 MP.L⁻¹ identified in the Gaussian model. As one of the criterion for a biomonitor is its ability to tolerate the target pollutant (Beeby 2001), further research is needed to define more precisely the tolerance range to MPs of freshwater mussels.

After 48 h of depuration, more than 50 % of MPs remain in freshwater mussels. Moderate to low MP depuration rates in dreissenid mussels have also been evidenced by Pedersen et al. (2020). Moreover, MPs can be retained in tissues of freshwater mussels for longer than one month (Merzel et al. 2020). Hence, the abundance of MPs in *Dreissena* spp. reflects an integrative process over time which can lead to a long-term accumulation of MPs, limiting their use to quantify the current MP pollution in freshwaters.

Both MP retention and impaired health status under high MP exposure suggest that dreissenids could rather be used as a strict bioindicator (i.e., organism reflecting the pollution state of the environment by changes in its presence/absence, physiology or behaviour (Gerhardt 2011)) to determine alert levels of environmental MP pollution, by assessing sublethal effects (e.g., valve opening, condition index) combined with MP quantification in tissues.

## 4.3. Comparison between the two mussel models

Depending on the exposure concentration, MP uptake in marine mussels was 4 to 34 times higher than in freshwater mussels, based on the number of MPs per individual. Moreover, the MP depuration rates were high for marine mussels whatever the initial exposure (from 88 to 97 %), but moderate and highly variable for dreissenid mussels (from 0 to 71 %). These differences are likely due to the size of the animals, which influence their nutritional needs, filtration rates (3.2 L hour⁻¹ for M. galloprovincialis (Sarà and Mazzola 2004) versus 0.4 L hour⁻¹ for dreissenid mussels (Baldwin et al. 2002)) and gut residence time. However, when comparing the number of MPs per dry weight, the quantity of MPs in dreissenids equals or exceeds that in marine mussels, suggesting a higher MP burden capacity in freshwater mussels. The difference observed between MP measured per individual or per dry weight can be explained by the fact that smaller organisms often have proportionally higher specific absorption due to a larger surface area to volume ratio, which increases the relative exchange surface area and can result in greater particle absorption per unit of tissue mass. Species-specific retention efficiency, or rates of particle elimination (e.g. pseudofaeces production) are also possible explanation. This may explain why dreissenids are more likely to be impacted by MPs under high environmental concentrations (2000 MPs.L⁻¹), resulting in
reduced MP uptake, whereas marine mussels appear unaffected, with MP uptake consistently increasing with exposure concentration.

We did not study the MP distribution in the different organs of *Dreissena* spp. mussels but it is likely that it would be similar to marine mussels as they are very similar biological models to *Mytilus* spp. (Binelli et al. 2015). Magni et al. (2018) found that 10 µm PS MPs can reach the digestive gland and the haemolymph of *D. polymorpha*, demonstrating the translocation of these beads inside the organism. Moreover, Peder-sen et al. (2020) found that 10 to 45 µm PE MPs largely accumulated in the intestines and gill tissues of quagga mussels. Nevertheless, while studying the MP distribution across tissues provides insights into their dynamics within mussels, analysing MPs at the whole-organism level is more relevant and practical for biomonitoring. This approach reduces the complexity as well as potential cross-contamination risks and MP loss associated with dissecting individual tissues.

## 4.4. Needs for future research

As a first step in evaluating their potential as biomonitors, mussels were exposed to fluorescent PE microspheres. These manufactured particles are practical for laboratory experiments and allowed an initial assessment of how MP uptake in mussels varies with water concentra-tion. However, this type of MPs may influence uptake and depuration processes, so the results should be interpreted with caution. Mussels may selectively filter fluorescent MPs, and the dyes used could alter MP surface properties, making them easier to adhere to mussel internal organs (Li et al. 2021). Further research is needed to compare fluores-cent particles with conventional polymers.

Furthermore, PE microbeads do not fully represent the diversity of MPs in natural ecosystems, where particles vary in size, shape, and chemical composition (Smith et al. 2018). Future studies should consider these factors to validate the use of mussels as MP biomonitors. For instance, particle size influences MP uptake, translocation, and egestion (Li et al. 2021). Moreover, most experimental studies focus on a single MP type, overlooking mussel preferences for different shapes (e.g., fibers, fragments, spheres, films) and polymer composition. Future studies should take into account this diversity in shape and composition of polymers on the MP uptake by bivalves. Finally, weathering and biofouling can alter MP uptake, as *M. galloprovincialis* has been found to ingest significantly more weathered PE MPs than virgin particles (Brâte et al., 2018a).

Toxicological investigations are required to further elucidate the biological effects induced by MPs and to assess how changes in health status influence mussels' capacity to maintain a stable uptake rate. Numerous studies have documented the impacts of elevated MP con-centrations on mussel biology, including physiological alterations (e.g., growth, reproduction, energy balance, immunity response) and shifts in gut microbial composition (Pittura et al., 2019; Shang et al., 2021; Park et al., 2024; Lan et al., 2025). These biological modifications may affect the bioaccumulation potential of MPs, as observed in *Dreissena* spp. under high-concentration exposure (Wolinski et al., 2025).

## 5. Conclusion

Our study highlights MP uptake by both *M. galloprovincialis* and *Dreissena* spp. mussels within 48 h, with MPs primarily found in the digestive gland of marine mussels. In the range of concentrations tested, the uptake of MPs in marine mussels is proportional to the MP con-centration in water, following a linear regression, while a Gaussian model better described the relationship for *Dreissena* spp. Marine mus-sels exhibit high MP depuration rates within 48 h in clean seawater, whereas dreissenid mussels show more moderate depuration rates. Our study suggests that smaller organisms may exhibit greater particle up-take per unit of tissue mass, due to a larger relative exchange surface area. Care should therefore be taken with regard to the unit of mea-surement used to compare organisms of different sizes, in order to avoid

drawing hasty conclusions. Although future research is needed on MP selectivity, uptake, and depuration by mussels, our study supports the use of marine mussels as efficient biomonitoring tools for MP levels at sea. In contrast, due to non-linear uptake patterns and high retention rates, freshwater mussels seem less effective as MP biomonitors but could be more suitable as strict bioindicators. These findings contribute to improving MP pollution assessment and developing new quantifica-tion tools. To go further, the health status of marine and freshwater mussels exposed to varying MP concentrations should be assessed to determine the threshold at which mussels transition from biomonitors to strict bioindicators.

## Funding

This work was supported by the French Ecological Transition Agency (MusselPlast SEA and MusselPlast RIVER projects). This work was part of the PhD thesis of A.W. supported by the CIFRE contract with the Plastic At Sea company, the National Research and Technology Agency and Sorbonne University.

## CRediT authorship contribution statement

**Adèle Wolinski:** Writing – review & editing, Writing – original draft, Visualization, Supervision, Methodology, Investigation, Formal analysis. **Miléna Ferret:** Investigation, Formal analysis. **Basile Bergeron:** Investigation, Formal analysis. **Loïc Tettling:** Methodology. **Edouard Lavergne:** Writing – review & editing, Visualization, Supervision, Project administration, Methodology, Investigation, Funding acquisition, Conceptualization. **Audrey M. Pruski:** Writing – review & editing, Methodology, Investigation, Conceptualization. **Isabelle Calvès:** Writing – review & editing, Methodology. **Anne-Leïla Meistertzheim:** Writing – review & editing, Supervision, Project administration, Methodology, Investigation, Funding acquisition, Conceptualization. **Franck Lartaud:** Writing – review & editing, Supervision, Project administration, Methodology, Investigation, Funding acquisition, Conceptualization.

## Declaration of competing interest

The authors declare the following financial interests/personal re- lationships which may be considered as potential competing interests:

Anne Leila Meistertzheim reports financial support was provided by SAS Plastic At Sea. Franck Lartaud reports financial support was pro- vided by Sorbonne University. Anne Leila Meistertzheim has patent PlastiCell(c) issued to BT8167PC00. If there are other authors, they declare that they have no known competing financial interests or per- sonal relationships that could have appeared to influence the work re- ported in this paper.

## Acknowledgements

The authors would like to thank Eva Lallemand, Noémie Massia and Jade Milelli for their help during mussel dissections. We are also grateful to the professional fishermen Cédric Giroud, and the divers of the Oce-anological Observatory of Banyuls-sur-Mer (OOB) Jean-Claude Roca and Bruno Hess, for supplying us in dreissenid and marine mussels. We would like to thank Pascal Romans, Nancy Trouillard and the aqua-riology department of the OOB for providing us the marine phyto-plankton and access to experimental laboratory conditions of OOB. We acknowledge the Biology Platform of Imaging and Cytometry (BioPIC) for access to microscope facilities. Finally we kindly thanks the two anonymous reviewer for their helpful comments to improve the manuscript.
## Supplementary materials

Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.aquatox.2025.107659.

## Data availability

Data will be made available on request.

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Further reading

Li, H., Ma, L., Lin, L., Ni, Z., Xu, X., Shi, H., Yan, Y., Zheng, G., Rittschof, D., 2018. Microplastics in oysters saccostrea CuCullata along the pearl river estuary, China. *Environ. Pollut.* 236 (May), 619–625. https://doi.org/10.1016/j.envpol.2018.01.083.