Next Article in Journal
The Relationship between Physical Fitness and Cognitive Functions in Older People: A Systematic Review
Previous Article in Journal
Evaluation of Topsoil Carbon Content and Quality in a Peatland and Reforested Soil after 50 Years of Soil Restoration in the Sierra de Guadarrama National Park (Spain)
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Sustainability
Volume 15
Issue 23
10.3390/su152316313
sustainability-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

First Report of Microplastic Ingestion in Edible Fish along Moroccan Mediterranean Coasts

by
Assia Bouzekry
1,
Bilal Mghili
1,
Oumayma Bouadil
2,
Monique Mancuso
3,
Mohamed Ben-Haddad
4,
Teresa Bottari
3,* and
Mustapha Aksissou
1
1
LESCB, URL-CNRST N° 18, Faculty of Sciences, Abdelmalek Essaâdi University, Tetouan 93000, Morocco
2
Laboratory of Applied Sciences, Environmental Management and Civil Engineering Research Team, ENSAH, Abdelmalek Essaâdi University, Tetouan 93000, Morocco
3
National Research Council (CNR), Institute for Marine Biological Resources and Biotechnology (IRBIM), 98122 Messina, Italy
4
Laboratory of Aquatic Systems: Marine and Continental Environments (AQUAMAR), Faculty of Sciences, Ibn Zohr University, Agadir 80000, Morocco
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(23), 16313; https://doi.org/10.3390/su152316313
Submission received: 21 October 2023 / Revised: 22 November 2023 / Accepted: 24 November 2023 / Published: 25 November 2023
(This article belongs to the Section Pollution Prevention, Mitigation and Sustainability)
Browse Figures
Versions Notes

Abstract

:
Monitoring the ingestion of microplastics (MPs) by marine organisms in the environment is essential for understanding the threats posed by these pollutants. In this study, we assessed, for the first time, the presence of MPs in the digestive tracts of two fish species, Chelon auratus and Sardina pilchardus, as well as a bivalve species, Callista chione, in the Moroccan Mediterranean Sea. Moreover, we calculated the polymeric hazard index (PHI) to verify the hazard level of isolated polymers. The results showed that all species ingested MPs, indicating a high level of MP pollution in this area. The MPs ingested were predominantly small (0.5–1 mm) and had a fiber-like shape. The results showed that PP and PET were the most abundant polymers ingested. The highest occurrence of MPs (100%) was found in C. chione and C. auratus, followed by S. pilchardus (72%). In C. chione, the average number of ingested MPs was 19.19 items per individual, while in C. auratus, the mean abundance of ingested MPs was 16.82 items per individual, and 9.64 items per individual in S. pilchardus. Moreover, the polymer hazard index showed that PET was in hazard level IV, while PP was in level III. Further studies are required in the Moroccan Mediterranean Sea to obtain a better evaluation of the occurrence, distribution, and impacts associated with MP pollution.

1. Introduction

In recent years, the production and consumption of plastic material has multiplied considerably. This, together with poor waste management, has created a high quantity of plastic waste, which is one of the most common types of anthropogenic pollution in the aquatic environment [1,2]. Plastic debris enters the ocean from a variety of sources, including those originating from activities at sea and on land. Furthermore, it can be transported for long distances before washing up on coastlines or settling on the seafloor [1].
Projections suggest that the production of plastic pollution will reach approximately 710 million tons in 2040 [3]. Alarmingly, by 2050, it is expected that the quantity of plastic debris in the ocean will exceed that of fish [4]. This trend will exacerbate its detrimental effects on ecosystems and marine biodiversity, as well as lead to substantial economic losses [5,6,7,8].
Once the plastic debris enters the marine ecosystem, it is progressively degraded physically (e.g., wind, wave actions, and mechanical transformation), chemically (e.g., photo-oxidation by solar radiation), and biologically, generating smaller pieces of plastic [9] called microplastics (MPs) (less than 5 mm in size). The accumulation of MPs in the oceans is an increasing threat to the aquatic ecosystem’s health [10]. MPs can be accidentally ingested by marine organisms because they mistake them for natural prey or they can be passively consumed during normal feeding behavior [11]. Ingested MPs can produce many negative impacts on marine organisms, including physiological disturbances [12], reproductive dysfunction [12], growth inhibition [13,14], biochemical alterations [15], blocking of the digestive tracts [16], decreased viability, and even mortality [17]. In addition, MPs can be a vector of harmful contaminants such as heavy metals and persistent organic pollutants (POPs) [18]. Finally, MPs can enhance the bioavailability of contaminants to organisms and ecosystems via adsorption and bioaccumulation [18].
Globally, the Mediterranean Sea is one of the regions most severely impacted by plastic pollution [19]. This basin is subjected to high levels of marine litter pollution due to its semi-enclosed nature, surrounded by three densely populated continents with approximately 150 million people, making it a sink for plastic litter [19]. Although it holds only 1% of the world’s water, the Mediterranean is the main hotspot for plastic waste, with 7% of global MPs [20]. Studies conducted in the Mediterranean documented up to 890,000 plastic items per km2 [21] most of which are MPs. In the Mediterranean Sea, the ingestion of microplastics was observed in a wide range of marine organisms, including mollusks, zooplankton, fish, seabirds, sea turtles, and cetaceans [22,23]. Moreover, it is important to highlight that there is a shortage of research documenting the MP abundances in marine organisms in the southern Mediterranean compared to the northern regions.
Extending along a coastline of over 500 km, Morocco’s Mediterranean region is widely used for several anthropic uses, such as fishing, shipping, tourism, and recreational activities. The human activities result in various consequences, including the presence of MPs [24]. The degree of pollution by marine litter found along the Moroccan Mediterranean Sea was identified as unacceptable [25,26,27]. Moroccan waters serve as feeding, refuge, and breeding grounds for numerous marine species (of which several are endangered species) that are important from both a commercial and environmental point of view [28]. Although there was an increase in research concerning MPs in the Moroccan marine environment [25,26,27,29], our understanding of the presence, ingestion, and consequences of marine litter in marine organisms remains limited. Due to the ubiquitous presence of MPs in the Moroccan Mediterranean and their multitude of effects on marine organisms, continuous monitoring of MPs in water and biota has been recommended [27]. Among the small pelagic fish species, the European sardine (Sardina pilchardus, Walbaum, 1792) is the most commercialized fish in the Moroccan Mediterranean and has accounted for up to 52% of total captures in recent years [30]. These fish represent a significant part of production and biomass and traditionally played a vital role in the ecosystem due to their strong coupling between demersal and pelagic ecosystems, where they are major prey for pelagic predators [31]. Additionally, they are largely distributed throughout the Mediterranean and have a selective feeding strategy [31,32]. The other important commercial fish in the Moroccan Mediterranean is the golden grey mullet, Chelon auratus (Risso, 1810). They are captured all along the Moroccan Mediterranean coast, and they are a considerable part of the local fish market [30]. This fish often enters the estuaries and mouths of rivers. This is a pelagic species that lives in shallow coastal and pelagic areas, at depths between 0 m and 20 m [33]. However, C. auratus usually follows an opportunistic feeding strategy and is marked by regular contact with the sediment, frequently distributed to the whole water column [33]. The smooth clam Callista chione (Linnaeus, 1758) is one of the main clam species commercialized in the Moroccan Mediterranean [34]. This species is largely distributed along the Moroccan Mediterranean coast, where it is caught by artisanal fishery fleets mainly in shallow coastal waters (5–25 m depth) on sandy to muddy bottoms [34]. In the Moroccan market, demand for this bivalve is always high and growing in summer by consumers. This sessile species filters a significant quantity of water and, consequently, absorbs and accumulates a wide range of marine toxins in the marine environment [35]. This means that C. chione is highly exposed to MPs with various densities. The selection of species studied involved organisms from different habitats, i.e., a sessile mollusk (bivalve) and two pelagic fish (the sardine and golden grey mullet), reflecting environmental conditions in various aquatic compartments. Besides their habitat differences, these species were selected for their feeding behavior (selective or non-selective), which can differently affect the ingestion and presence of MPs in their bodies. In the Mediterranean, the smooth clam and sardine are among the suggested indicators for MPs due to their wide commercial importance, spatial distribution, feeding strategies, and habitat, as well as documented MP ingestion [22].
Given the scarcity of data about MPs ingested by marine species in Morocco, this study aimed (i) to detect, quantify and characterize MPs in three edible species: the two fish species C. auratus and S. pilchardus and the bivalve species C. chione; and (ii) to evaluate the polymer hazard index (PHI) in order to obtain information about the danger of any polymer for the marine environment and human health.

2. Materials and Methods

2.1. Study Area and Samplings

Samplings were conducted during September and October 2022 at three different locations in the Moroccan Mediterranean: Martil (Lat. 35°37′37.266″ N, Long. 5°16′8.886″ W), M’diq (Lat. 35°41′16.341″ N, Long. 5°18′41.121″ W), and Fnideq (Lat. 35°50′23.462″ N, Long. 5°21′1.607″ W) (see Figure 1).
Fish samples were captured using a trawl measuring 45 m to 60 m in width and 250 m to 300 m in length, with a mesh size of 1 cm. For shellfish specimens, a trawl measuring 1.5 m in length and 1 m in width, with a mesh size of 1.5 cm, was used. Trawling activities at each site were carried out for a duration of 30 min at an approximate speed of 2 knots. The sampling depths ranged from 20 to 60 m for fish and from 10 to 13 m for shellfish. In total, we collected 35 samples of C. auratus, 50 of S. pilchardus, and 46 of C. chione. The fish and shellfish were promptly placed into aluminum bags and transported to the Chemistry Laboratory at the National Institute of Fisheries Research in Tangier, Morocco, using a cooler maintained at a temperature of 4 °C. Upon arrival at the laboratory, the samples were stored at −30 °C until analysis.

2.2. Microplastic Isolation

The methodology of this study adheres to the most recent recommendations for research on MPs [36]. In the laboratory, prior to the analysis, each sample was gradually thawed overnight at 4 °C. Then, each fish specimen was measured for total length (TL, cm) and total weight (TW, g). The gastrointestinal tract (GIT), from the esophagus to the end of the intestine, was removed, weighed, transferred to a conical glass flask, and treated with a 10% KOH solution at a ratio of 1:5 (w/v). In the same way, each shellfish specimen was measured (shell length, cm) and weighed (whole body). Regarding the shellfish, each individual was carefully dissected, and all flesh, including the digestive system, was weighed and transferred into a glass flask with a 10% KOH (Sigma Aldrich, Merck, Darmstadt, Germany) solution at a ratio of 1:5 (w/v). Each flask was covered with aluminium foil and stirred at 40 °C for 48 h [36]. After this period each sample was placed in a glass cylinder, and a hypersaline 15% NaCl solution was added in order to obtain density separation of the two phases and to collect the floating MPs. Then, the supernatant was transferred to a filtration system with a stainless-steel funnel (YT-330B, Winteam, Hangzhou, China) and filtered through a fiberglass filter (pore size 1 µm, 47 mm, Whatman, Stuttgart Germany). The filter membranes were then placed in Petri dishes and dried at 40 °C for 24 h. After that, the filters were placed in sterile glass Petri dishes and observed under a stereomicroscope. All suspected microparticles were counted, measured, and photographed.

2.3. Quality Control and Preventing Contamination

To avoid contamination during laboratory assays, rigorous precautions were followed according to Bottari et al. [11]. All samples were processed in a room with restricted access, to prevent any accidental external contamination. All workspaces and tools were cleaned with ethanol and filtered deionized water to prevent any particle contamination. Only glassware was used. Operators’ hands and forearms were cleaned before the procedure, and white cotton lab coats (100% cotton), latex gloves, and masks were used during sample handling and processing. All the solutions (Milli-Q water, KOH, NaCl) were pre-filtered at 0.2 μm (Whatman cellulose nitrate membrane filters, diameter of 47 mm) using a vacuum glass filtration apparatus kit prior to use. The procedures were performed under a laminar hood. To mitigate the risk of airborne contamination, procedural blanks were introduced using a 10% KOH solution. In order to maintain accuracy and prevent an overestimation of MP content, filters dampened with moisture were placed in glass Petri dishes and put under the microbiological hood and next to the microscope.

2.4. Polymer Identification

A total of 23 MP particles were randomly selected and analyzed using Raman spectroscopy. The use of Raman spectroscopy for the identification of MPs has recently increased due to the precise characterization and its ability to count micrometer-sized items [11]. Raman spectra were quantified using an HR Evolution micro-confocal Raman system (Horiba Scientific, Kyoto, Japan) with a DXR 532 nm laser diode and a 10× Olympus objective. Spectra were generated with wavenumbers of 600 to 4000 cm−1, while the number of spectra accumulations and the duration of laser exposure ranged from 2 to 20 and from 5 to 20 s, respectively, based on the specific dye in the MP. The laser power was regulated below 5 mW to prevent particle photo-degradation. The spectra obtained were characterized by comparing them with those of standard materials listed in the spectral databases of the Bio-Rad KnowItAll Spectral Library and the Spectral Library of Plastic Particles (SLoPP and SLoPP-E).

2.5. Polymer Hazard Index (PHI)

The polymer hazard index (PHI) was employed to assess the potential threat posed by these MPs to human health.
The PHI was calculated with the following formula [37]:
PHI = ∑Pn × Sn
where Pn is the percentage of specific polymer types detected in edible fish and Sn is the hazard score of polymers developed by Lithner et al. [37]. The PHI was determined following the method of Nithin et al. [38]. PHI was sorted into different hazard levels as reported by Lithner et al. [37]. Based on the values obtained, five hazard levels were given (I = 0–1; II = 1–10; III = 10–100; IV = 100–1000; and V > 1000).

2.6. Data Analysis

The abundance of MPs in this study was expressed as MPs/individual. Descriptive analysis was performed examining mean MP abundance, standard deviation, and percentage of MP characteristics. The Kruskal–Wallis test was used to compare MP abundance between the three species and between the three sampling stations. Pearson’s Chi-squared was applied to check significant associations between MP size, color, and shape between the three species. Statistical tests were carried out with IBM SPSS Statistics 20 software. Statistical significance was determined at 0.05.

3. Results

3.1. MPs Abundance

A total of 131 specimens were assessed. The length and weight of the golden grey mullet (C. auratus) sampled varied from 20 to 29.2 cm with an average of 22.54 cm and 64.79 to 178 g with a mean of 91.22 g, respectively (Table 1). The European pilchard (S. pilchardus), weight recorded ranged from 54 to 98 g, with an average of 74.35 g, and a length from 19.4 to 24 cm, with an average of 21.52 cm (Table 1). The smooth clam (C. chione), showed a size between 5.5 and 7.8 cm (mean = 6.90 cm) which corresponds to a weight between 10 and 44.23 g (mean = 21.90 g).
The results showed that 1.954 suspected items were ingested/accumulated by the three species: 883 in C. chione, 589 in C. auratus, and 482 in S. pilchardus. The photographs of MPs detected in fish and bivalves are shown in Figure 2.
The highest frequency of occurrence was observed in the bivalve C. chione (100%, n = 46). Regarding fish, C. auratus showed 100% (n = 35) MP ingestion, while S. pilchardus showed 72% (n = 32, Table 1).
In C. chione, the average number of ingested/accumulated MPs was 19.19 items/individual. For the fish species, C. auratus exhibited an average of 16.82 items/individual, while S. pilchardus had an average of 9.64 items/individual.
The Kruskal–Wallis test indicated that there were no significant differences in the number of ingested MPs among the three species (H = 2, p > 0.05).
C. chione specimens collected from the Martil station showed the highest number of MPs per individual (22.52 items/individual). Finally, specimens collected from the M’diq and Fnideq stations showed a significant MP abundance of 18.37 items/individual and 16.28 items/individual, respectively.
In the case of S. pilchardus, the abundance of ingested MPs was higher in samples from the Fnideq station (15.85 items/individual) than in the M’diq station (9.06 items/individual).
The percentage of ingested/accumulated MPs, size, shape, and color categories did not differ between the three species (Pearson’s chi-square test, p > 0.05).
The microplastics detected in the examined marine organisms exhibited a range of shapes, with fibers being the most common at 80.60%, followed by fragments (17.70%) and foam (1.70%). No pellets or films were found. Fibers were dominant for both fish and bivalve species (93–95% and 65%, respectively) (Figure 3). Fragments constituted 31% in bivalve samples and between 5 and 7% in fish samples. Foams were only observed in C. chione specimens sampled in the M’diq and Fnideq stations (1.31 and 10.20%, respectively).
Regarding the colors, more than half of MPs were found to be black (56.34%), followed by yellow (12.43%), blue (11.05%), red (8.80%), transparent (4%), grey (2.91%), violet (1.07%), green (0.61%), and orange (0.10%) (Figure 4). The black color was predominant in all three species: 72.36% in C. auratus, 60.80% in S. pilchardus, and 43% for C. chione.
The MPs detected in the three species were categorized into five groups: 0.5–1 mm, 1–2 mm, 2–3 mm, 3–4 mm, and 4–5 mm. The overall average size of MPs recorded in this study was 0.91 mm. Among the size classes observed, MPs within the 0.5–1 mm range were the most prevalent, constituting 68.83% of the total. This was followed by 1–2 mm (20.90%), 2–3 mm (6.34%), 3–4 mm (2.76%), and 4–5 mm (1.17%) (Figure 5a). This study highlights that MPs ranging from 0.5 to 1 mm were very abundant at all the sampling sites, Martil (77.46%), M’diq (64.13%), and Fnideq (60.36%). However, 4–5 mm sized MPs were high in the M’diq station, with 3.18% (Figure 5).
Results showed that the most represented MP size category was the 0.5–1 mm range, with a percentage of 71.18% in C. auratus, 69.08% in S. pilchardus, and 63.95% in C. chione. Remarkably, bivalve specimens tended to ingest/accumulate larger sizes of MPs than the fish (3–5 mm). The average size of MPs observed in C. chione was 0.95 mm, while the average size in the two fish species was 0.86 mm. No significant differences in the size of the MPs ingested were observed between the three species according to the Kruskal–Wallis test (p < 0.05).

3.2. Polymer Composition and Risk Assessment

The assay performed by Raman spectroscopy identified five types of plastic polymers. These include Polypropylene (PP), Polyethylene terephthalate (PET), Polyvinyl chloride (PVC), Polyethylene (PE), and polycarbonate (PC). Examples of MPs observed in the biota studied with the corresponding Raman spectra are shown in Figure A1. As shown in Figure 6, the most prevalent polymer detected was PP (39.14%), followed by PET (26.08%), PVC (17.40%), PE (8.69%), and PC (8.69%).
PHI values for the identified polymers ranged from 10.22 (PC) to 183.46 (PVC), with a total PHI of 432.72, indicating a hazard level of IV (100–1000). Only PP (39.13) was in the moderate risk category (Table 2). PE (95.59) and PP had a PHI ranging from 10 to 100, placing them in the hazard category III, which denotes a high risk. Finally, PVC (183.46) and PET (104.32) had a PHI ranging from 100 to 1000, placing them in the hazard category IV.

4. Discussion

The rate of plastic pollution along the Moroccan Mediterranean coast is rising alarmingly [28], but, currently, knowledge about the ingestion of microplastics by marine organisms is limited. This study aimed to investigate the occurrence, abundance, and chemical composition of MPs ingested/accumulated by three edible marine organisms at three locations in the Moroccan Mediterranean Sea. The presence of hazardous polymers for human and marine environment was also studied by calculating the PHI.
Although the number of microplastics examined and characterized is limited, this is the first study conducted on fish and shellfish along the Moroccan Mediterranean coastline. These initial findings are very important as not only do they shed light on the presence of this pollution, but they also offer valuable information on the type of pollutants present.
The abundance of MPs varied among the three species. The habitat preferences of marine biota could influence the ingestion of MPs [39]. Based on their habitat preferences, C. auratus and S. pilchardus were categorized as pelagic fish, while C. chione was classified as a benthic species. The highest concentrations of MPs were observed in C. chione (19.19 MPs/ind). This result is expected since bivalves feed through sediment filtration, resulting in a higher intake of MP particles, linked to the fact that MPs/NPs tend to sink to the seafloor [40,41]. Bivalve species possess the ability to filter and accumulate MPs of various sizes, with the levels depending on the abundance and distribution of MPs in the water [40]. C. chione is a shallow-burrowing benthic suspension feeder [34,35] that lives on sandy bottoms in coastal waters at depths varying from 1 to 180 m, although it is more common between 5 and 10 m depths on the Martil coast and other regions studied [34]. Several studies highlighted the presence of high concentrations of MPs in bivalves, especially in edible clams, mussels, and oysters [40,41,42,43]. The average number of ingested MPs in C. chione (19.19 items/individual) is similar to the values recorded in bivalves in China (24.64 items/individual, Wu et al. [44]), Iran (21.8 items/individual, Abbasi et al. [45]), and Vietnam (30.67 items/individual, Thanh et al. [46]). However, the values found were higher than those observed by Rios-Fuster et al. [47] in the western Mediterranean (4.83 items/individual), in Spain (4.54–18.2 items/individual, Capo et al. [40]), Tunisia (7.7 items/individual, Wakkaf et al. [48]), and Italy (3.95 ± 2.54 items/individual, Nalbone et al. [41]). Finally, our results are lower than values recorded in India (91.42 items/individual, Naidu et al. [43]) and in the Mediterranean coasts of Turkey (39.15 items/individual, Atici [42]. Due to their feed habits and habitat, this group of invertebrates offers optimal ecological characteristics to be a bioindicator species for monitoring MPs in the marine environment [48].
The intake and ingestion of MPs can differ among marine species due to the variations in their feeding behavior. C. chione is a filter-feeder and can accidentally ingest suspended items, so this non-selective feeding behavior could explain the high levels of MPs found in this study. In our study, C. auratus was found to have the highest quantity of MPs in their digestive tract compared to S. pilchardus. The diet of C. auratus consists of small benthic organisms, unicellular algae, and occasionally plankton [33]. This opportunistic feeding strategy used by C. auratus may expose them to high levels of MP ingestion. This aspect makes C. auratus more prone to ingesting MPs dispersed throughout the water column. Furthermore, C. auratus enters and feeds near rivers, increasing the risk of MP ingestion. Depending on their feeding strategies, European sardines have a highly selective diet [31,32] and rarely consume MPs, which explains the low percentage of ingestion by this species compared to C. auratus. It is the only species, among the examined animals, that feeds exclusively on pelagic organisms. The differences in ingestion and intake of MPs between the three species may have been caused by variations in the concentration of MPs in the surrounding water in which the species live. However, by decreasing the MP size, fish ingestion can rise due to their incapacity to differentiate between MPs and food [44]. The method of contamination probably plays an important role in the differences observed in the three species. For example, the fish’s original prey may already be polluted with MP via false ingestion, secondary consumption, or trophic transfer [49]. However, it should not be forgotten that MPs ingested by these marine species can accumulate in predatory species that eat these contaminated species [50]. Bioaccumulation of MPs happens when their uptake from the marine ecosystems by all possible routes—i.e., ingestion and contact, from all possible sources—i.e., sediments, water, or prey [50]. Bioaccumulation and subsequent trophic transfer of MPs can lead to biomagnification of these pollutants at higher trophic levels [50]. MPs can also increase the bioavailability of contaminants to marine organisms through bioaccumulation [18].
The occurrence of MPs in C. auratus was studied by a limited number of researchers (Table 3). Güven et al. [51] showed an average of 7.47 items/individual, similar to values (6.66 items/individual) found in Egypt (Mediterranean Sea) [52] (Table 3), while in Tunisia, Abidli et al. [53] recorded the presence of MPs in 87% of C. auratus specimens studied, with values higher than our results (65.33 items/individual in the Bizerte lagoon and 42 items/individual in the Ghar El Melh lagoon). In this study, MP abundances in S. pilchardus (9.64 items/individual) were higher than those recorded by Filgueiras et al. [54] (1.77 items/individual) in the NW Iberian shelf, and by Rios-Fuster et al. [47] (0.44 items/individual) in Spain. Also, Kermenidou et al. [55] reported lower values than our results (2.5 items/individual) in the Thermaic Gulf (North Aegean Sea), as well as Savoca et al. [56], who detected 0.53 items/individual in the Southern Tyrrhenian Sea, and Anastasopoulou et al. [57], who reported 0.8 items/individual in the Eastern Ionian Sea (see Table 3).
By contrast, the MP concentrations recorded in S. pilchardus were comparable to those recorded in the same species in the Adriatic Sea (4.63 items/individual), Italy (6.21 items/individual, Trani et al. [58]), and Spain (8.62 items/individual, Sánchez-Guerrero-Hernández et al. [59]).
Table 3. Summary of microplastic concentrations in Chelon auratus and Sardina pilchardus along the Mediterranean coasts.
Table 3. Summary of microplastic concentrations in Chelon auratus and Sardina pilchardus along the Mediterranean coasts.
Sampling AreaSpeciesNFO (%)N Items/IndividualPolymerIdentification MethodReferences
Eastern Ionian SeaChelon auratus20959.5--Anastasopoulou et al. [57]
Northern Levant SeaChelon auratus39363PE, PPFT-IRGüven et al. [51]
Northern TunisiaChelon auratus10-65.3PP, PEFT-IRAbidli et al. [53]
Northern Adriatic SeaSardina pilchardus10251.4PVC, PS, PPFT-IRAvio et al. [60]
Alboran Sea; Northern Spain; Gulf of LionSardina pilchardus10533.30–0.5PET, PA, PE, cellophane, cotton, woolFTIRCompa et al. [61]
Northern Adriatic SeaSardina pilchardus99191.8PE, PET, PS, PVC, NylonFT-IRAvio et al. [62]
Northern Adriatic SeaSardina pilchardus8096---Renzi et al. [63]
Northern Adriatic SeaSardina pilchardus30370.9--Anastasopoulou et al. [57]
Eastern Ionian SeaSardina pilchardus36470.8--Anastasopoulou et al. [57]
Northern Levant SeaSardina pilchardus7-2.7PE, PPFT-IRGüven et al. [51]
Northern SpainSardina pilchardus15871.8PE, PPµRamanFilgueiras et al. [54]
Northern SpainSardina pilchardus7-0.1--Rios-Fuster et al. [47]
Northern Spain; Gulf of LionSardina pilchardus104581.1–1.8--Pennino et al. [64]
Gulf of LionSardina pilchardus13-0.5PEFT-IRConstant et al. [23]
North Aegean SeaSardina pilchardus--2.5--Kermenidou et al. [55]
Southern Tyrrhenian SeaSardina pilchardus19-0.5PP, PAN, PE, PARaman, FT-IRSavoca et al. [56]
Frequency of occurrence: FO; Number of specimens: N; Polyethylene: PE; Polypropylene: PP; Polyvinyl Chloride: PVC; Polyamide: PA; Polyacrylonitrile: PAN; Polystyrene: PS; Polyethylene terephthalate: PET.
Differences between MP abundances recorded in the Moroccan Mediterranean Sea compared to other studies may be due to several factors. Firstly, these differences may arise from variations in the methods used for MP extraction. Secondly, the varying levels of MP pollution in the study sites and the subsequent ingestion of microplastics by marine organisms could be contributing factors. For instance, certain areas might exhibit a higher concentration of wastewater treatment plants [65], estuaries [66], or the influence of large coastal cities [24,65], all of which have a notable impact on the marine environment.
The three locations selected for our study are severely affected by tourism, as previously reported by Mghili et al. [29], who classified them as extremely dirty. In fact, off the coasts of the Moroccan Mediterranean Sea, there are several wastewater treatment plants discharging into the sea. MP ingestion and intake incidence was higher in samples from Martil than in Fnideq and M’diq, indicating a relationship between MP bioavailability and proximity to urban centers. In addition, Martil receives a high amount of input from the Martil River, and this could explain the high number of MPs found in the studied species in this region. Moreover, the high abundance of MPs in the Moroccan beach sediments provides further evidence of the level of pollution in this region. In addition, the high abundance of plastic litter on the seafloor, regularly observed in bottom trawl fishing, could explain the rising incidences of ingestion of MPs in the three examined species [27]. Also, Alshawafi et al. [24] indicated that the highest concentrations of MPs were recorded near the most populated metropolitan areas in the Moroccan Mediterranean. A strong correlation between MP density in water and MP density in marine organisms has already been reported [66].
The ingestion of MPs by marine species is affected by their sizes, shapes, and colors, as well as by their source [67]. Our findings indicated that the major MP shape found was fiber. This result is in accordance with the studies conducted in the Iberian Peninsula by Bellas et al. [68], Compa et al. [61], Lopes et al. [69], Filgueiras et al. [54], and Pennino et al. [64], as well as in Portugal by Neves et al. [70], where fibers constitute over 60% of the MPs found. A similar pattern was observed in studies conducted in Tunisia [53] and Egypt [52]. Several studies revealed that fibers are the most common in the ecosystem marine, such as sea surface waters, seabeds, and in the gastrointestinal tracts of invertebrates and vertebrates [22,57,68]. Microfibers were reported to be widely ingested by aquatic species because they are often mistaken as prey [71]. In our study, we also found high levels of fiber ingestion. These fibers are probably a consequence of the degradation of ropes and fishing nets, as well as the washing of synthetic clothing [72]. These synthetic textiles account for 35% of the global release of primary microplastics into the marine environment [72], and can be ingested by aquatic biota [8], as also reported in recent studies that highlighted the MPs’ ubiquity in the Moroccan marine environment [24].
Regarding the color of microplastics, it plays a crucial role in influencing the probability of ingestion by marine organisms. In our study, we observed that black and blue were the dominant color in all three species, constituting a range of 12–63%. Our results are supported by previous studies, such as those reported by Abidli et al. [53] in Tunisia, Hamed et al. [73] in Egypt, and Kılıç et al. [74] in Turkey, as well as, Bellas et al. [68], on the Spanish Mediterranean and Atlantic coasts. Moreover, our findings are in accordance with Matluba et al. [75] and Zhang et al. [39] in Bangladesh and in the East China Sea, respectively. Compa et al. [61], on the Mediterranean coast of the Iberian Peninsula, showed that blue and transparent particles were the most frequent colors. On the contrary, Filgueiras et al. [54] highlighted that sardine and anchovy specimens from the western Cantabrian Sea ingested a predominance of transparent items. These differences may be attributed to the prevalence of these colors in the environment or to the selectivity in targeting particles that resemble their natural prey [67].
Moreover, this study highlighted that small MPs were the most dominant in all three species (0.5–1 mm), as previously reported by Bellas et al. [68] in fish species from the Spanish Mediterranean and Atlantic coasts, and Filgueiras et al. [54] in pelagic and benthic fish from the northwestern Iberian Plateau. The average size of MPs obtained in the Gulf of Cadiz by Sánchez-Guerrero-Hernández et al. [59] was 0.92 mm for sardines and 0.88 mm for anchovies. Similarly, Lopes et al. [69] observed the dominance of the size class below 0.50 mm, while Filgueiras et al. [54] reported slightly higher average sizes (i.e., 1.46 mm for sardines), and the most common size class was 0.5–1 mm. Finally, the average size of MPs in fish and water in the South China Sea was less than 0.5 mm [71].
The polymer characterization performed by Raman showed a total of five polymer types: PP, PET, PVC, PE, and PC. These polymers have been recognized as the most common plastics contaminating the marine environment due to their wide range of applications and durability [76]. This finding is in line with what Suaria et al. [20] reported, highlighting the prevalence of PP (polypropylene) and PE (polyethylene) in the Mediterranean surface waters [77] and emphasizing that these two polymers represent 62% of global plastic demand. Similar findings were also recorded by Abidli et al. [53] in fish in Tunisia and by Neves et al. [70] in commercial fish off the Portuguese coast. One of the most likely sources of MPs (PP and PET) in water environments is fishing gear. The use of plastic ropes and fishing nets in the Moroccan Mediterranean coasts is a probable source of MPs in the marine biota in this region. Discarded clothing also contributes to MP pollution in Moroccan waters. PP and PE microfibers have been linked to textile washing activities.
Finally, the PHI results showed that PVC and PET had the highest PHI, indicating that their release into the water could have serious harmful effects not only on marine life but also on human health [38]. In contrast, PP had the lowest PHI, suggesting that it represents a relatively lower risk. Although the hazard of ingesting MPs is high, our results are preliminary, and further studies on PHI are needed to better understand the potential risk to human and marine environmental health. In Morocco, fish represent the most important source of protein consumed by the population and, therefore, can serve as the main exposure route of MPs and associated pollutants for many people. Sardines remain the most important fishery product, with national production surpassing 850,000 tonnes per year, being the most common species in Morocco in terms of biomass, catches, and consumption. Finally, sardines represent more than half of total Moroccan fisheries’ production (52%) [30]. Similarly, C. chione is a commercially important species on many coasts of the Moroccan Mediterranean. Due to the significant consumption of this species, the presence of microplastics in bivalves poses a potential risk to human health. In particular, most species of bivalves are consumed whole, which can increase human exposure to MPs. In contrast, the risk of ingestion and intake of MPs in fish is mitigated by the removal of the gastrointestinal tract in most species. However, when humans consume polluted species, it can result in the bioaccumulation of MP [50]. Moreover, the exposure to chemical contaminants associated with MPs has become a serious issue, given that chemical bioaccumulation in marine biota can reach human consumers [18].
One of the main limitations of this study is the low percentage of MPs analyzed by Raman spectrometry. Further studies would be required for more vigorous detection of MP concentrations. To achieve these objectives, it is important to use more specific technology (i.e., μ-FTIR and μ-Raman) in future studies in Morocco to detect small-sized MPs.

5. Conclusions

This study assesses, for the first time, the contamination by MPs in three edible marine organisms off the coast of Tetouan in the Mediterranean Sea. The observed concentrations significantly exceed those reported in prior studies conducted in the Mediterranean Sea. The bivalve C. chione was more sensitive to MP intake than others, suggesting that the different behavior strategies and feeding play a crucial role in determining the ingestion of these contaminants. The main limitations of this study include its restricted sampling period, which does not consider seasonal variations, and the lack of comparative studies, which prevents the investigation of correlations between MP abundance in biota and in water and sediments. This paper also highlights the occurrence and potential risks of MPs in ocean food webs and for human health. It emphasizes the need for additional studies on the sources of MP pollution and the impact of these pollutants on marine species. In light of these findings, it is strongly recommended to expand the scope of research to encompass a broader array of species and habitats, facilitating a comprehensive assessment of MP pollution concentrations in marine organisms within the Moroccan Mediterranean. Additionally, measures should be implemented to prevent the accumulation of MP pollutants in Moroccan coastal water.

Author Contributions

Conceptualization, A.B. and B.M.; Formal analysis, A.B., B.M. and M.B.-H.; Methodology, A.B., B.M., O.B. and T.B.; Supervision, M.M., T.B. and M.A.; Validation, B.M., M.B.-H. and M.A.; Writing—original draft, A.B., B.M., O.B. and M.M.; Writing—review and editing, B.M., M.M. and T.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A

Sustainability 15 16313 g0a1
Figure A1. Examples of Raman spectra of samples analyzed. (a): Polypropylene and (b): Polyvinyl Chloride.
Figure A1. Examples of Raman spectra of samples analyzed. (a): Polypropylene and (b): Polyvinyl Chloride.
Sustainability 15 16313 g0a1

References

  1. Jambeck, J.R.; Geyer, R.; Wilcox, C.; Siegler, T.R.; Perryman, M.; Andrady, A.; Narayan, R.; Law, K.L. Plastic waste inputs from land into the ocean. Science 2015, 347, 768–771. [Google Scholar] [CrossRef] [PubMed]
  2. De-la-Torre, G.E.; Dioses-Salinas, D.C.; Pizarro-Ortega, C.I.; Santillàn, L. New plastic formations in the Anthropocene. Sci. Total Environ. 2021, 754, 142216. [Google Scholar] [CrossRef] [PubMed]
  3. Lau, W.W.Y.; Shiran, Y.; Bailey, R.M.; Cook, E.; Stuchtey, M.R.; Koskella, J.; Velis, C.A.; Godfrey, L.; Boucher, J.; Murphy, M.B.; et al. Evaluating scenarios toward zero plastic pollution. Science 2020, 369, 1455–1461. [Google Scholar] [CrossRef] [PubMed]
  4. MacArthur, D.E.; Waughray, D.; Stuchtey, M.R. The New Plastics Economy, Rethinking the Future of Plastics; World Economic Forum: Geneva, Switzerland; Ellen MacArthur Foundation: Isle of Wight, UK, 2016. [Google Scholar]
  5. Krelling, A.P.; Williams, A.T.; Turra, A. Differences in perception and reaction of tourist groups to beach marine debris that can influence a loss of tourism revenue in coastal areas. Mar. Policy 2017, 85, 87–99. [Google Scholar] [CrossRef]
  6. Beaumont, N.J.; Aanesen, M.; Austen, M.C.; Börger, T.; Clark, J.R.; Cole, M.; Hooper, T.; Lindeque, P.K.; Pascoe, C.; Wyles, K.J. Global ecological, social and economic impacts of marine plastic. Mar. Pollut. Bull. 2019, 142, 189–195. [Google Scholar] [CrossRef] [PubMed]
  7. Kühn, S.; van Franeker, J.A. Quantitative overview of marine debris ingested by marine megafauna. Mar. Pollut. Bull. 2020, 151, 110858. [Google Scholar] [CrossRef]
  8. Roman, L.; Schuyler, Q.; Wilcox, C.; Hardesty, B.D. Plastic pollution is killing marine megafauna, but how do we prioritize policies to reduce mortality? Conserv. Lett. 2021, 14, e12781. [Google Scholar] [CrossRef]
  9. Browne, M.A.; Crump, P.; Niven, S.J.; Teuten, E.; Tonkin, A.; Galloway, T.; Thompson, R. Accumulation of microplastic on shorelines woldwide: Sources and sinks. Environ. Sci. Technol. 2011, 45, 9175–9179. [Google Scholar] [CrossRef]
  10. Derraik, J.G.B. The Pollution of the Marine Environment by Plastic Debris: A Review. Mar. Pollut. Bull. 2002, 44, 842–852. [Google Scholar] [CrossRef]
  11. Bottari, T.; Mancuso, M.; Pedà, C.; De Domenico, F.; Laface, F.; Schirinzi, G.F.; Battaglia, P.; Consoli, P.; Spanò, N.; Greco, S.; et al. Microplastics in the bogue, Boops boops: A snapshot of the past from the southern Tyrrhenian Sea. J. Hazard. Mater. 2022, 424, 127669. [Google Scholar] [CrossRef]
  12. Rochman, C.M.; Kurobe, T.; Flores, I.; Teh, S.J. Early warning signs of endocrine disruption in adult fish from the ingestion of polyethylene with and without sorbed chemical pollutants from the marine environment. Sci. Total Environ. 2014, 493, 656–661. [Google Scholar] [CrossRef]
  13. Besseling, E.; Wang, B.; Lürling, M.; Koelmans, A.A. Nanoplastic affects growth of S. obliquus and reproduction of D. magna. Environ. Sci. Technol. 2014, 48, 12336–12343. [Google Scholar] [CrossRef] [PubMed]
  14. Welden, N.A.C.; Cowie, P.R. Long-term microplastic retention causes reduced body condition in the langoustine, Nephrops norvegicus. Environ. Pollut. 2016, 218, 895–900. [Google Scholar] [CrossRef] [PubMed]
  15. Contino, M.; Ferruggia, G.; Pecoraro, R.; Scalisi, E.M.; Cavallaro, G.; Bonaccorso, C.; Fortuna, C.G.; Salvaggio, A.; Capparucci, F.; Bottari, T.; et al. Uptake routes and biodistribution of polystyrene nanoplastics on zebrafish larvae and toxic effects on development. Fishes 2023, 8, 168. [Google Scholar] [CrossRef]
  16. Lei, L.; Wu, S.; Lu, S.; Liu, M.; Song, Y.; Fu, Z.; Shi, H.; Raley-Susman, K.M.; He, D. Microplastic particles cause intestinal damage and other adverse effects in zebrafish Danio rerio and nematode Caenorhabditis elegans. Sci. Total Environ. 2018, 619–620, 1–8. [Google Scholar] [CrossRef] [PubMed]
  17. Mallik, A.; Xavier, K.M.; Naidu, B.C.; Nayak, B.B. Ecotoxicological and Physiological Risks of Microplastics on Fish and Their 511 Possible Mitigation Measures. Sci. Total Environ. 2021, 779, 146433. [Google Scholar] [CrossRef]
  18. Amelia, T.S.M.; Khalik, W.M.; Ong, M.C.; Shao, Y.T.; Pan, H.; Bhubalan, K. Marine microplastics as vectors of major ocean pollutants and its hazards to the marine ecosystem and humans. Prog. Earth Planet Sci. 2021, 8, 12. [Google Scholar] [CrossRef]
  19. Cózar, A.; Sanz-Martín, M.; Martí, E.; González-Gordillo, J.I.; Ubeda, B.Á.; Gálvez, J.; Irigoien, X.; Duarte, C.M. Plastic accumulation in the Mediterranean Sea. PLoS ONE 2015, 10, e0121762. [Google Scholar] [CrossRef]
  20. Suaria, G.; Avio, C.G.; Mineo, A.; Lattin, G.L.; Magaldi, M.G.; Belmonte, G.; Moore, C.J.; Regoli, F.; Aliani, S. The Mediterranean plastic soup: Synthetic polymers in Mediterranean surface waters. Sci. Rep. 2020, 6, 37551. [Google Scholar] [CrossRef]
  21. Eriksen, M.; Lebreton, L.C.M.; Carson, H.S.; Thiel, M.; Moore, C.J.; Borerro, J.C.; Galgani, F.; Ryan, P.G.; Reisser, J. Plastic pollution in the world’s oceans: More than 5 trillion plastic pieces weighing over 250,000 tons afloat at sea. PLoS ONE 2014, 9, e111913. [Google Scholar] [CrossRef]
  22. Fossi, M.C.; Pedà, C.; Compa, M.; Tsangaris, C.; Alomar, C.; Claro, F.; Ioakeimidis, C.; Galgani, F.; Hema, T.; Deudero, S.; et al. Bioindicators for monitoring marine litter ingestion and its impacts on Mediterranean biodiversity. Environ. Pollut. 2018, 237, 1023–1040. [Google Scholar] [CrossRef] [PubMed]
  23. Constant, M.; Reynaud, M.; Weiss, L.; Ludwig, W.; Kerhervé, P. Ingested Microplastics in 18 Local Fish Species from the Northwestern Mediterranean Sea. Microplastics 2021, 1, 186–197. [Google Scholar] [CrossRef]
  24. Alshawafi, A.; Analla, M.; Alwashali, E.; Aksissou, M. Assessment of marine debris on the coastal wetland of Martil in the North-East of Morocco. Mar. Pollut. Bull. 2017, 117, 302–310. [Google Scholar] [CrossRef] [PubMed]
  25. Loulad, S.; Houssa, R.; El Ouamari, N.; Rhinane, H. Quantity and spatial distribution of seafloor marine debris in the Moroccan Mediterranean Sea. Mar. Pollut. Bull. 2019, 139, 163–173. [Google Scholar] [CrossRef] [PubMed]
  26. Bouzekry, A.; Mghili, B.; Aksissou, M. Addressing the challenge of marine plastic litter in the Moroccan Mediterranean: A citizen science project with schoolchildren. Mar. Pollut. Bull. 2022, 184, 114167. [Google Scholar] [CrossRef] [PubMed]
  27. Mghili, B.; Keznine, M.; Hasni, S.; Aksissou, M. Abundance, composition and sources of benthic marine litter trawled-up in the fishing grounds on the Moroccan Mediterranean coast. Reg. Stud. Mar. Sci. 2023, 63, 103002. [Google Scholar] [CrossRef]
  28. Mghili, B.; Keznine, M.; Analla, M.; Aksissou, M. The impacts of abandoned, discarded and lost fishing gear on marine biodiversity in Morocco. Ocean Coast Manag. 2023, 239, 106593. [Google Scholar] [CrossRef]
  29. Mghili, B.; Lamine, I.; Bouzekry, A.; Gunasekaran, K.; Aksissou, M. Cigarette butt pollution in popular beaches of Morocco: Abundance, distribution, and mitigation measures. Mar. Pollut. Bull. 2023, 195, 115530. [Google Scholar] [CrossRef]
  30. MPM. Rapport d’activité Ministère des Pêches Maritimes Maroc; Ministère de l’Agriculture, de la Pêche Maritime, du Développement Rural et des Eaux et Forêts: Rabat, Morocco, 2018. [Google Scholar]
  31. Chen, C.-T.; Carlotti, F.; Harmelin-Vivien, M.; Bănaru, D. Temporal variation in prey selection by adult European sardine (Sardina pilchardus) in the NW Mediterranean Sea. Prog. Oceanogr. 2021, 196, 102617. [Google Scholar] [CrossRef]
  32. Costalago, D.; Palomera, I. Feeding of European pilchard (Sardina pilchardus) in the northwestern Mediterranean: From late larvae to adults. Sci. Mar. 2014, 78, 41–54. [Google Scholar] [CrossRef]
  33. Kesiktaş, M.; Yemişken, E.; Yildiz, T.; Eryilmaz, L. Age, growth and reproduction of the golden grey mullet, Chelon auratus (Risso, 1810) in the Golden Horn Estuary, Istanbul. J. Mar. Biolog. Assoc. U. K. 2020, 100, 989–995. [Google Scholar] [CrossRef]
  34. Bouzaidi, H.; Maatouk, M.; El Moumni, B.; Haroufi, O.; Saber, M.A.; AbouElmaaty, E.E.; Daoudi, M. Population structure, age and growth of Callista chione (Bivalvia: Veneridae) in Martil Coast of the western Mediterranean. Reg. Stud. Mar. Sci. 2021, 48, 101996. [Google Scholar] [CrossRef]
  35. Baeta, M.; Solís, M.; Ramon, M.; Ballesteros, M. Effects of fishing closure and mechanized clam dredging on a Callista chione bed in the western Mediterranean Sea. Reg. Stud. Mar. Sci. 2021, 48, 102063. [Google Scholar] [CrossRef]
  36. Dehaut, A.; Hermabessiere, L.; Duflos, G. Current frontiers and recommendations for the study of microplastics in seafood. Trac. Trends Anal. Chem. 2019, 116, 346–359. [Google Scholar] [CrossRef]
  37. Lithner, D.; Larsson, Å.; Dave, G. Environmental and health hazard ranking and assessment of plastic polymers based on chemical composition. Sci. Total Environ. 2011, 409, 3309–3324. [Google Scholar] [CrossRef] [PubMed]
  38. Nithin, A.; Sundaramanickam, A.; Iswarya, P.; Babu, O.G. Hazard index of microplastics contamination in various fishes collected off Parangipettai, Southeast coast of India. Chemosphere 2022, 307, 136037. [Google Scholar] [CrossRef] [PubMed]
  39. Zhang, F.; Xu, J.; Zhu, L.; Peng, G.; Jabeen, K.; Wang, X.; Li, D. Seasonal distributions of microplastics and estimation of the microplastic load ingested by wild caught fish in the East China Sea. J. Hazard. Mater. 2021, 419, 126456. [Google Scholar] [CrossRef]
  40. Capo, X.; Rubio, M.; Solomando, A.; Alomar, C.; Compa, M.; Sureda, A.; Deudero, S. Microplastic intake and enzymatic responses in Mytilus galloprovincialis reared at the vicinities of an aquaculture station. Chemosphere 2021, 280, 130575. [Google Scholar] [CrossRef]
  41. Nalbone, L.; Cincotta, F.; Giarratana, F.; Ziino, G.; Panebianco, A. Microplastics in fresh and processed mussels sampled from fish shops and large retail chains in Italy. Food Control 2021, 125, 108003. [Google Scholar] [CrossRef]
  42. Atici, A.A. The first evidence of microplastic uptake in natural freshwater mussel, Unio stevenianus from Karasu River, Turkey. Biomarkers 2022, 27, 118–126. [Google Scholar] [CrossRef]
  43. Naidu, B.C.; Xavier, K.A.M.; Shukla, S.P.; Jaiswar, A.K.; Nayak, B.B. Comparative study on the microplastics abundance, characteristics, and possible sources in yellow clams of different demographic regions of the northwest coast of India. J. Hazard. Mater. Lett. 2022, 3, 100051. [Google Scholar] [CrossRef]
  44. Wu, Y.; Yang, J.; Li, Z.; He, H.; Wang, Y.; Wu, H.; Xie, L.; Chen, D.; Wang, L. How does bivalve size influence microplastics accumulation? Environ. Res. 2022, 214, 113847. [Google Scholar] [CrossRef] [PubMed]
  45. Abbasi, S.; Soltani, N.; Keshavarzi, B.; Moore, F.; Turner, A.; Hassanaghaei, M. Microplastics in different tissues of fish and prawn from the Musa Estuary, Persian Gulf. Chemosphere 2018, 205, 80–87. [Google Scholar] [CrossRef] [PubMed]
  46. Thanh, N.D.; Thu, V.A.; Thom, D.T.; Manh, D.T.; Tuan, P.M.; Ngo, V.D.; Van Tuyen, T. Investigation of microplastics existence in mussel (Perna viridis) from Ha Long bay, Viet Nam. Vietnam J. Sci. Technol. 2022, 60, 1–10. [Google Scholar]
  47. Rios-Fuster, B.; Alomar, C.; Compa, M.; Guijarro, B.; Deudero, S. Anthropogenic particles ingestion in fish species from two areas of the western Mediterranean Sea. Mar. Pollut. Bull. 2019, 144, 325–333. [Google Scholar] [CrossRef] [PubMed]
  48. Wakkaf, T.; El Zrelli, R.; Kedzierski, M.; Balti, R.; Shaiek, M.; Mansour, L.; Tlig-Zouari, S.; Bruzaud, S.; Rabaoui, L. Microplastics in edible mussels from a southern Mediterranean lagoon: Preliminary results on seawater-mussel transfer and implications for environmental protection and seafood safety. Mar. Pollut. Bull. 2020, 158, 111355. [Google Scholar] [CrossRef] [PubMed]
  49. Horton, A.A.; Jürgens, M.D.; Lahive, E.; van Bodegom, P.M.; Vijver, M.G. The influence of exposure and physiology on microplastic ingestion by the freshwater fish Rutilus rutilus (roach) in the River Thames, UK. Environ. Pollut. 2018, 236, 188–194. [Google Scholar] [CrossRef]
  50. Miller, M.E.; Hamann, M.; Kroon, F.J. Bioaccumulation and biomagnification of microplastics in marine organisms: A review and meta-analysis of current data. PLoS ONE 2020, 15, e0240792. [Google Scholar] [CrossRef]
  51. Güven, O.; Gökdağ, K.; Jovanović, B.; Kıdeyş, A.E. Microplastic litter composition of the Turkish territorial waters of the Mediterranean Sea, and its occurrence in the gastrointestinal tract of fish. Environ. Pollut. 2017, 223, 286–294. [Google Scholar] [CrossRef]
  52. Sayed, A.E.H.; Hamed, M.; Badrey, A.E.A.; Ismail, R.F.; Osman, Y.A.A.; Osman, A.G.M.; Soliman, H.A.M. Microplastic distribution, abundance, and composition in the sediments, water, and fishes of the Red and Mediterranean seas, Egypt. Mar. Pollut. Bull. 2021, 173, 112966. [Google Scholar] [CrossRef]
  53. Abidli, S.; Akkari, N.; Lahbib, Y.; Trigui El Menif, N. First evaluation of microplastics in two commercial fish species from the lagoons of Bizerte and Ghar El Melh (Northern Tunisia). Reg. Stud. Mar. Sci. 2021, 41, 101581. [Google Scholar] [CrossRef]
  54. Filgueiras, A.V.; Preciado, I.; Cartón, A.; Gago, J. Microplastic ingestion by pelagic and benthic fish and diet composition: A case study in the NW Iberian shelf. Mar. Pollut. Bull. 2020, 160, 111623. [Google Scholar] [CrossRef]
  55. Kermenidou, M.; Frydas, I.S.; Moschoula, E.; Kousis, D.; Christofilos, D.; Karakitsios, S.; Sarigiannis, D. Quantification and characterization of microplastics in the Thermaic Gulf, in the North Aegean Sea. Sci. Total Environ. 2023, 892, 164299. [Google Scholar] [CrossRef] [PubMed]
  56. Savoca, S.; Bottari, T.; Fazio, E.; Bonsignore, M.; Mancuso, M.; Luna, G.M.; Romeo, T.; D’Urso, L.; Capillo, G.; Panarello, G.; et al. Plastics occurrence in juveniles of Engraulis encrasicolus and Sardina pilchardus in the Southern Tyrrhenian Sea. Sci. Total Environ. 2020, 718, 137457. [Google Scholar] [CrossRef]
  57. Anastasopoulou, A.; Viršek, M.K.; Varezic, D.B.; Digka, N.; Fortibuoni, T.; Koren, S.; Mandic, M.; Mytilineou, C.; Pesic, A.; Ronchi, F.; et al. Assessment on marine litter ingested by fish in the Adriatic and NE Ionian Sea macro-region (Mediterranean). Mar. Pollut. Bull. 2018, 133, 841–851. [Google Scholar] [CrossRef]
  58. Trani, A.; Mezzapesa, G.; Piscitelli, L.; Mondelli, D.; Nardelli, L.; Belmonte, G.; Toso, A.; Piraino, S.; Panti, C.; Baini, M.; et al. Microplastics in water surface and in the gastrointestinal tract of target marine organisms in Salento coastal seas (Italy, Southern Puglia). Environ. Pollut. 2023, 316, 120702. [Google Scholar] [CrossRef] [PubMed]
  59. Sánchez-Guerrero-Hernández, M.J.; González-Fernández, D.; Sendra, M.; Ramos, F.; Yeste, M.P.; González-Ortegón, E. Contamination from microplastics and other anthropogenic particles in the digestive tracts of the commercial species Engraulis encrasicolus and Sardina pilchardus. Sci. Total Environ. 2023, 860, 160451. [Google Scholar] [CrossRef] [PubMed]
  60. Avio, C.G.; Pittura, L.; d’Errico, G.; Abel, S.; Amorello, S.; Marino, G.; Gorbi, S.; Regoli, F. Distribution and characterization of microplastic particles and textile microfibers in Adriatic food webs: General insights for biomonitoring strategies. Environ. Pollut. 2020, 258, 113766. [Google Scholar] [CrossRef]
  61. Compa, M.; Ventero, A.; Iglesias, M.; Deudero, S. Ingestion of microplastics and natural fibres in Sardina pilchardus (Walbaum, 1792) and Engraulis encrasicolus (Linnaeus, 1758) along the Spanish Mediterranean coast. Mar. Pollut. Bull. 2018, 128, 89–96. [Google Scholar] [CrossRef]
  62. Avio, C.G.; Gorbi, S.; Regoli, F. Experimental development of a new protocol for extraction and characterization of microplastics in fish tissues: First observations in commercial species from Adriatic Sea. Mar. Environ. Res. 2015, 111, 18–26. [Google Scholar] [CrossRef]
  63. Renzi, M.; Specchiulli, A.; Blašković, A.; Manzo, C.; Mancinelli, G.; Cilenti, L. Marine litter in stomach content of small pelagic fishes from the Adriatic Sea: Sardines (Sardina pilchardus) and anchovies (Engraulis encrasicolus). Environ. Sci. Pollut. Res. 2019, 26, 2771–2781. [Google Scholar] [CrossRef] [PubMed]
  64. Pennino, M.G.; Bachiller, E.; Lloret-Lloret, E.; Albo-Puigserver, M.; Esteban, A.; Jadaud, A.; Bellido, J.M.; Coll, M. Ingestion of microplastics and occurrence of parasite association in Mediterranean anchovy and sardine. Mar. Pollut. Bull. 2020, 158, 111399. [Google Scholar] [CrossRef] [PubMed]
  65. Rajan, K.; Khudsar, F.A.; Kumar, R. Spatio-temporal patterns of microplastic contamination in surface waters of Hooghly River Estuary: Causes and consequences. Reg. Stud. Mar. Sci. 2023, 65, 103111. [Google Scholar] [CrossRef]
  66. Qu, X.; Su, L.; Li, H.; Liang, M.; Shi, H. Assessing the relationship between the abundance and properties of microplastics in water and in mussels. Sci. Total Environ. 2018, 621, 679–686. [Google Scholar] [CrossRef] [PubMed]
  67. Lopes Costa, L.; da Costa, I.D.; da Silva Oliveira, A.; Rosental Zalmon, I. “Microplastic ecology”. Testing the influence of ecological traits and urbanization in microplastic ingestion by sandy beach fauna. Estuar. Coast. Shelf Sci. 2023, 290, 108406. [Google Scholar] [CrossRef]
  68. Bellas, J.; Martínez-Armental, J.; Martínez-Cámara, A.; Besada, V.; MartínezGómez, C. Ingestion of microplastics by demersal fish from the Spanish Atlantic and Mediterranean coasts. Mar. Pollut. Bull. 2016, 109, 55–60. [Google Scholar] [CrossRef]
  69. Lopes, C.; Raimundo, J.; Caetano, M.; Garrido, S. Microplastic ingestión and diet composition of planktivorous fish. Limnol. Oceanogr. Lett. 2020, 5, 103–112. [Google Scholar] [CrossRef]
  70. Neves, D.; Sobral, P.; Ferreira, J.L.; Pereira, T. Ingestion of microplastics by commercial fish off the Portuguese coast. Mar. Pollut. Bull. 2015, 101, 119–126. [Google Scholar] [CrossRef]
  71. Nie, H.; Wang, J.; Xu, K.; Huang, Y.; Yan, M. Microplastic pollution in water and fish samples around Nanxun Reef in Nansha Islands, South China Sea. Sci. Total Environ. 2019, 696, 134022. [Google Scholar] [CrossRef]
  72. Boucher, J.; Friot, D. Primary Microplastics in the Oceans: A Global Evaluation of Sources; IUCN: Gland, Switzerland, 2017; 43p. [Google Scholar]
  73. Hamed, M.; Martyniuk, C.J.; Lee, J.S.; Shi, H.; Sayed, A.E. Distribution, abundance, and composition of microplastics in market fishes from the Red and Mediterranean seas in Egypt. J. Sea Res. 2023, 194, 102407. [Google Scholar] [CrossRef]
  74. Kılıç, E. Microplastic ingestion evidence by economically important farmed fish species from Turkey. Mar. Pollut. Bull. 2022, 183, 114097. [Google Scholar] [CrossRef] [PubMed]
  75. Matluba, M.; Ahmed, M.K.; Chowdhury, K.M.A.; Khan, N.; Ashiq, M.A.; Islam, M.S. The pervasiveness of microplastic contamination in the gastrointestinal tract 563 of fish from the western coast of Bangladesh. Mar. Pollut. Bull. 2023, 193, 115145. [Google Scholar] [CrossRef] [PubMed]
  76. Erni-Cassola, G.; Zadjelovic, V.; Gibson, M.I.; Christie-Oleza, J.A. Distribution of plastic polymer types in the marine environment; A meta-analysis. J. Hazard Mater. 2019, 369, 691–698. [Google Scholar] [CrossRef] [PubMed]
  77. Andrady, A.L. Persistence of Plastic Litter in the Oceans. In Marine Anthropogenic Litter; Bergmann, M., Gutow, L., Klages, M., Eds.; Springer: Cham, Switzerland, 2015; pp. 57–72. [Google Scholar]
Sustainability 15 16313 g001
Figure 1. Geographical map of sampling area in the Moroccan Mediterranean.
Figure 1. Geographical map of sampling area in the Moroccan Mediterranean.
Sustainability 15 16313 g001
Sustainability 15 16313 g002
Figure 2. Examples of MP types found in the three species.
Figure 2. Examples of MP types found in the three species.
Sustainability 15 16313 g002
Sustainability 15 16313 g003
Figure 3. Percentage of MP shapes representing all three species (a) and among species (b).
Figure 3. Percentage of MP shapes representing all three species (a) and among species (b).
Sustainability 15 16313 g003
Sustainability 15 16313 g004
Figure 4. Percentage of MP colors representing all three species (a) and among species (b).
Figure 4. Percentage of MP colors representing all three species (a) and among species (b).
Sustainability 15 16313 g004
Sustainability 15 16313 g005
Figure 5. Percentage of MP sizes representing all three species (a) and among species (b).
Figure 5. Percentage of MP sizes representing all three species (a) and among species (b).
Sustainability 15 16313 g005
Sustainability 15 16313 g006
Figure 6. MP polymers detected in edible fish.
Figure 6. MP polymers detected in edible fish.
Sustainability 15 16313 g006
Table 1. Number (N) of specimens, mean, standard deviation of total length (TL, cm) and total weight (TW, g), frequency of occurrence (FO), and relative abundance (MPs/ind).
Table 1. Number (N) of specimens, mean, standard deviation of total length (TL, cm) and total weight (TW, g), frequency of occurrence (FO), and relative abundance (MPs/ind).
Species NHabitatMean TL, cmMean TW, gFO (%)MPs/ind
Chelon auratus35Pelagic22.54 ± 1.7091.22 ± 21.0410016.82
Sardina pilchardus50Pelagic21.52 ± 1.1174.35 ± 11.52729.64
Callista chione46Benthic6.90 ± 0.7921.90 ± 9.0010019.19
Table 2. Polymers detected are categorized according to hazard level and polymer hazard index (PHI).
Table 2. Polymers detected are categorized according to hazard level and polymer hazard index (PHI).
PolymerMonomerHazardHazard LevelScorePHIHazard CategoryRisk Category
PPPropyleneHarmful when inhaled.I139.13IIIHigh
PETEthylene glycolHarmful if swallowed.II4104.32IVVery High
PVCVinyl chlorideExtremely flammable gas; May cause cancer.V10.5183.46IVVery High
PEEthyleneExtremely flammable gas; May cause drowsiness or dizziness.II1195.59IIIHigh
PCBisphenol AMay cause an allergic skin reaction; Suspected of damaging fertility or the unborn child; May cause drowsiness or dizziness.IV1.210.22IIModerate
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Bouzekry, A.; Mghili, B.; Bouadil, O.; Mancuso, M.; Ben-Haddad, M.; Bottari, T.; Aksissou, M. First Report of Microplastic Ingestion in Edible Fish along Moroccan Mediterranean Coasts. Sustainability 2023, 15, 16313. https://doi.org/10.3390/su152316313

AMA Style

Bouzekry A, Mghili B, Bouadil O, Mancuso M, Ben-Haddad M, Bottari T, Aksissou M. First Report of Microplastic Ingestion in Edible Fish along Moroccan Mediterranean Coasts. Sustainability. 2023; 15(23):16313. https://doi.org/10.3390/su152316313

Chicago/Turabian Style

Bouzekry, Assia, Bilal Mghili, Oumayma Bouadil, Monique Mancuso, Mohamed Ben-Haddad, Teresa Bottari, and Mustapha Aksissou. 2023. "First Report of Microplastic Ingestion in Edible Fish along Moroccan Mediterranean Coasts" Sustainability 15, no. 23: 16313. https://doi.org/10.3390/su152316313

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop