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Article

The Use of Zebra Mussel (Dreissena polymorpha) as a Sentinel Species for the Microplastic Pollution of Freshwater: The Case of Beyhan Dam Lake, Turkey

by
Muhammed Atamanalp
1,
Mine Kokturk
2,
Fatih Gündüz
3,
Veysel Parlak
4,
Arzu Ucar
1,
Duried Alwazeer
5,6,7 and
Gonca Alak
8,*
1
Department of Aquaculture, Faculty of Fisheries, Atatürk University, Erzurum 25030, Turkey
2
Department of Organic Agriculture Management, Faculty of Applied Sciences, Igdir University, Igdir 76000, Turkey
3
Fisheries Research Institute, Elazığ 23000, Turkey
4
Department of Basic Sciences, Faculty of Fisheries, Ataturk University, Erzurum 25030, Turkey
5
Research Center for Redox Applications in Foods (RCRAF), Igdir University, Igdir 76000, Turkey
6
Innovative Food Technologies Development, Application, and Research Center, Igdir University, Igdir 76000, Turkey
7
Department of Nutrition and Dietetics, Faculty of Health Sciences, Igdir University, Igdir 76000, Turkey
8
Department of Seafood Processing, Faculty of Fisheries, Atatürk University, Erzurum 25030, Turkey
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(2), 1422; https://doi.org/10.3390/su15021422
Submission received: 29 November 2022 / Revised: 9 January 2023 / Accepted: 9 January 2023 / Published: 11 January 2023
(This article belongs to the Special Issue Pollution and Toxicology of Aquatic Ecosystems)
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Abstract

:
The presence of microplastics (MPs) in several components of different ecosystems has aroused great concern and led to numerous studies on MP pollution. Although there has been an increasing number of these studies in aquatic ecosystems, no data about the MP pollution in zebra mussel (Dreissena polymorpha, Pallas 1771) living in Beyhan dam lake (Elazığ, Türkiye) are available. This study aimed to investigate the presence of MPs in freshwater mussel species found in this water reservoir. The distribution and characterization of MPs were investigated by Fourier transform infrared spectroscopy (FTIR) in zebra mussel (D. polymorpha) samples at four different stations. A significant difference in the MP presence between the 1st and 4th stations was observed (p < 0.05). A total of 52 MPs were determined in mussels collected from different stations in Beyhan Dam Lake. A total of 18 MPs of this total (1.80 ± 0.92 MP/individual) were obtained in station 1 and 7 of them (0.70 ± 0.82 MP/individual) were from the 4th station. Results of the MP investigation showed that the dominant color was black, the common size range was 1001–2000 µm, the dominant polymer shape was fiber, and the main polymer type was polypropylene (PP). A positive correlation was found among total MP and factors (length, tissue weight, and MP/individual). The detection of MPs in a freshwater mussel of the Beyhan dam lake can be suggested as a threat indicator and offers the possibility of using D. polymorpha as a bioindicator in the aquatic ecosystems’ MP pollution.

Graphical Abstract

1. Introduction

Microplastics (MPs) found at high levels in aquatic environments are considered a serious pollution problem for ecosystems [1,2,3,4,5]. In this sense, some organisms represent an effective tool in monitoring programs for the assessment and monitoring of environmental quality in both freshwater and marine environments. Of these organism groups, those that are easier to sample and give more effective results are preferred. It has been recommended to use organisms such as mussels in risk assessments to characterize environmental-induced changes and toxicological pathways in the aquatic ecosystem [6]. Mussel biomarkers have been proposed to be used as early warning signals of environmental quality due to their sensitive tissue, exposure time, and many other factors [7]. Zebra mussels, Dreissena polymorpha (Pallas, 1771) are one of two species of freshwater shellfish distributed in Eastern Europe, North America, and Western Asia [8]. It has always aroused interest among scientists due to its neotenic properties (byssus and planktonic larval stage) that enable it to easily penetrate aquatic ecosystems and form colonies that invade water pumps, channels, channel walls, and bottoms. These species can change the aquatic ecosystems’ ecology by rapidly creating a large population as well as the energy flow in the food chain due to their feeding through filtration. Because of this feeding behavior, Zebra mussels can concentrate pollutants in their bodies even when these pollutants are found at low levels in an environment. Filtration nutrition pumps large volumes of water and concentrates many xenobiotics including microplastics in their tissues. These substances are then propagated and amplified through the food chain [9].
Dreissena polymorpha is an excellent model organism for in situ monitoring and ecotoxicological experiments of MPs as well as different pollutants. Due to their biology, it has a high filtration rate and is now a species found in water reservoirs in different parts of Europe [9,10,11]. Although Dreissena polymorpha ingests suspended particles up to ~40 μm in size, this bivalve has an inhalant siphon with a diameter of about 1 mm that can ingest particles even larger than 40 μm [12]. This mussel species (Dreissena polymorpha) generally spreads in lakes and reservoirs in Turkey. It is known that female mussels can produce millions of eggs per individual during the spawning period and the zebra mussel population has greatly increased in the last ten years in Turkish inland waters [8]. Dreissena polymorpha is considered a harmful invasive epibiont species as it blocks water flow in hydroelectric and nuclear power systems. Moreover, this species has been reported with positive effects in cleaning water, removing turbidity, and filtering pollutants, and has benefits on the population of some fish and aquatic species [13]. Dreissena polymorpha is widely used in ecotoxicological experiments due to its strong oxidative defense and relatively high resistance to xenobiotics [14]. Using the bioindicators is not limited to a single species which has limited environmental tolerance. All communities which have large environmental tolerance can serve as bioindicators and can be helpful for determining the environmental situation with “biotic index” or “multimetric” [15].
The present study aimed to evaluate the potential use of D. polymorpha as an MP pollution bioindicator of freshwater ecosystems as well as to reveal the extent of MP pollution of aquatic ecosystems, especially in freshwater. Another aim was to highlight the initial data on zebra mussels regarding the detection rates, and characterization of MPs, and provide a model of association with each other.

2. Materials and Methods

2.1. Study Area

Beyhan Dam and Hydroelectric Power Plant (HEPP) is located 15 km East of the Palu district center and 2.5 km Northeast of Beyhan Town (Palu, Elazığ, Türkiye). The dam, which started working in 2015 and has a body volume of 1,350,000 m3, contributes to meeting the energy need. Mussel samples were collected from 4 different stations determined in Beyhan Dam lake (1. Station: 38.7543379° N 40.1446659° E, 2. Station: 38.7516595° N 40.1426613° E, 3. Station: 38.7403259° N 40.2231718° E and 4. Station: 38.7231310° N 40.3696191° E, Figure 1). A total of 10 zebra mussels (Dreissena polymorpha) for each station were brought to laboratories in laptop coolers supplemented with ice cassettes.

2.2. Sampling

Zebra mussels (D. polymorpha) were collected from the identified stations in October 2022 (Figure 1). The mussels (Figure 2) (n = 10 per station, 40 in total) were collected with D-shaped stainless-steel nets and cotton gloves [16]. They were wrapped in aluminum foil, placed in plastic ziplock bags and transported to the laboratory in a cooler box and frozen at −20 °C before microplastic extraction. Before processing the mussels, all surfaces and equipment were cleaned with MilliQ water and ethanol. The mussels were thawed at room temperature and the shells were cleaned with MilliQ water and dried with a paper towel. The shell lengths of the mussels were measured with a digital caliper and weighed after removing the soft tissue from the shells (Table 1).

2.3. Observation and Validation of Microplastic

In order to prevent contamination in our study, the floor, tools and glass materials on which my work was carried out were cleaned with ethanol and filtered pure water. The materials used throughout the study were covered or closed with aluminum foil. A white cotton apron and gloves were worn, especially for fiber MP contamination, which may be caused by clothing. The protocol for the evaluation of microplastics in some marine life samples was used with a few modifications [17,18]. Wet tissues after weighting were placed in glass beakers and 10% potassium hydroxide (KOH) (10 mL (w/v)) was added. The beakers were then sealed with aluminum foil and placed in a shaken incubator at 60 °C and 120 rpm for 6 h to complete the digestion of the organic material. After the digestion period, the remaining part was filtered through glass fiber filters (Whatman GF/C) using a vacuum pump. The filters were put in glass petri and incubated for 24 h at 60 °C. Four procedural cavities, i.e. samples without mussel tissue, were used to assess micro-plastic contamination of the samples filter paper left open during the study in 2 petri dishes as blanks [19].
The dried filters were examined under a stereomicroscope at 40× magnification, with microplastics characterized by color (blue, black, red, and grey/whitish) and shape (fiber and fragment). In cases where the visual evaluation was not sufficient, the hot needle technique was used to confirm microplastic formation. The hot needle method is used in only 10% of the samples and is used to avoid the risk of misidentification of colored fibers [20]. Microplastic dimensions (50–100 μm, 101–200 μm, 201–300 μm, 301–500 μm, 501–1000 μm, 1001–2000 μm, 2001–3000 μm and 3001–5000 μm) in the pictures were recorded under the microscope and measured using the ImageJ software program. The count of microplastics was calculated both per individual and per 1 gram. The blanks contained an average of 0.5 ± 0.6 fragments of the four, only two black fragments were found on the filter papers in the exposed petri dishes. Evaluations were made by subtracting the amount of MP in the blank from all mussel samples. No fiber or pellet MP was found in the blank [21]. The MPs found in the blank samples were common polymers such as polypropylene (PP). More than 10% of the identified MPs were used in Fourier transform infrared spectroscopy (Agilent Cary 630 FTIR Spectrometer, Agilent, Santa Clara, CA, USA) to investigate the spectral signal exchange of polymers in the wavelength range of 4000 to 650 cm−1. The polymer types of the MPs were taken from the Agilent MicroLab FTIR software library. The spectra of the samples were compared with library data, and samples with more than 70% spectral similarity were accepted [22].

2.4. Data Analysis

A one-way analysis of variance (ANOVA) was used to determine differences in MP quantities between stations, shape, size, and color distribution. Post-hoc Tukey was applied to test multiple comparisons. A significance level of 0.05 was chosen. The correlation analysis was conducted to specify the direction and strength of these relationships. Statistical analyses were performed with GraphPad Prism 8 program.

3. Results and Discussion

A total of 52 MPs were determined in mussels collected from different stations in Beyhan Dam Lake (Table 1). A significant difference in the presence of MPs in Zebra mussels at different stations was observed only at the 1st and 4th stations (p < 0.05) (Figure 3).
It is often difficult to determine the sources and course of MPs, especially in inland waters, because MP abundance varies spatially [16]. However, in the obtained findings, it is thought that the filtration rate of D. polymorpha is effective depending on the ground structure and water flow status of the stations in the difference between the stations. The filtration rate in large D. polymorpha individuals was lower than in smaller mussels due to age-related degeneration [9].
Accordingly, the presence of MPs in stations 2, 3, and 4 were consistent with the findings (2–14 total items) of Pastorino et al. [9] on the same species. The results of station 1 show that large anthropogenic activities and nearby urban areas can lead to an increase in water-borne microplastics [1,23]. Considering the correlation table, it is seen that there is a positive correlation between the factors. However, the correlation between total MP—length and total MP—tissue weight was found to be insignificant (Table 2). The relationship between bivalve size and MP ingestion is unclear and research has not found any significant correlation among body size, length, weight and MP ingestion rate [24]. This situation is in line with our current study findings.
Furthermore, in the present research, the findings showed that large mussels contain more MP than small ones when evaluated in terms of total MP presence. This situation has been confirmed by Kallenbach et al. [24]. In addition, the same researcher reported the potential of bivalve species to represent viable bioindicators in freshwater systems and remarked the necessity of further research is to understand the thresholds and relationships for organism size and MP uptake.
Bivalves are valuable sentinel organisms in determining the levels of different pollutants in the environment due to their pollutant accumulate ability. Organisms fed by filtration are known to accumulate pollutants with low excretion rates [6]. Reguera et al. [25], found the mean concentration of MP (2.55 ± 2.80 MP g−1 WW) in mussels (Mytilus spp.) of the Cantabrian Sea (Spain) higher than Ria of Vigo’s mussels (1.59 ± 1.28 MP g−1 WW).
In our study, the dominant color of MPs found in all stations was black (site 1; 55.6%, site 2; 50.0%, site 3; 63.6, site 4; 85.7%) (Figure 4A). In contrast to our findings, it has been reported that white, light-colored and transparent fibers were the dominant MPs [10,26]. It has been reported that since mussels cannot selectively uptake fibers based on color, the shown color ratio may represent a true picture of the proportion of dyed fibers in the edible size range, although the color of ingested MPs may also be seasonal [27]. However, in another report claimed that mussels may have a color preference to feed and that the color distribution of MPs in mussels may be a result of both the color preference of the mussels and the dominant color in water [28]. Unlike our results, Ding et al. [29] reported the seasonal effect on MP uptake by mussels, with bivalves being more transparent in autumn and summer, bluer in winter, and equal amounts of both MPs in spring.
The dimensions of the microplastics detected in mussel tissues were found to be in the range of 1001–2000 μm (Station 2; 50.0%, Station 3; 45.5%) (Figure 4B). Similar to our research findings, Pe et al. [30] found the highest percentage of MP size ranging from 1001 to 2000 μm. Size contributes to the perception of prey, and MPs with a similar size, as those found in the natural food chain, are more likely to be ingested by the organism [2,3]. Additionally, larger particles are probably difficult to expel and tend to stay in mussels for longer times. Moreover, longer fibers can become entangled in the gastrointestinal tract and therefore are difficult to remove from the body [31].
The understanding of the MPs’ eco-toxicological effects is also limited by the different sizes and shapes of MPs and the different additives used in plastics production which complicate studies on these effects [23]. During the filtration process, mussels take in not only phytoplankton, bacteria, organic matter, but also sand and silt particles, as well as indigestible microplastics (fragments, films and fibers). Changes in the environment are often attributed to anthropogenic adverse events (e.g., pollution, land use changes) or natural stressors (e.g., drought, freezing in late spring). However, if MP levels increase in the future, it may increase the adverse environmental effects of multiple anthropogenic stressors. Therefore, this study was designed as an initial study in this region to integrate the MP presence into ecotoxicology studies in assessing the environmental adverse effects on freshwater ecosystems. However, concerns have been expressed about potential impacts on biota as microplastics (MP) are ubiquitous in aquatic ecosystems and may be one of the anthropogenic stress factors [32]. In our study, the dominant polymer shape in the mussel tissues was found to be fiber for all stations (Figure 5A,B). In particular, the presence of 100% fiber-type polymers was found in the 2nd and 4th stations (Figure 5A). The presence of high amounts of fiber in mussels might be due to the ecology/biology of the mussels and the high amount of fiber discharged from homes into rivers [27]. Shape differences (fiber, fragment, etc.) and concentrations of MPs can affect the filtration rate and accordingly the feeding activity in mussels (bivalves) [33]. Atıcı [34] reported that fiber was the most MP found in bivalves, which agrees with our research findings.
FTIR analysis of 28.8% (15 of them) of the identified MPs was performed (Figure 6A). The results show that there were 53.3% polypropylene (PP), 33.3% copolymer ethyl-acrylate (COPOLY) and 13.3% polychloroprene (Neoprene) polymer types (Figure 6B).
Our findings show that types of plastics differ in diversity and abundance. However, there are no experimental data in the literature to compare the MP amount stored in mussel species collected from the same environmental conditions. Gündoğdu et al. [35] reported that plastics have a large surface area and structure allowing them to be attached to organisms. The fact that PP was the most dominant MP type might be due to the structure of the hydroelectric power plant located in the Beyhan Dam Lake. In all geomorphic structures, PP, PE and to a lesser extent PS are the majority polymers [36]. The density of MP polymers can result from the different water layers of the reservoir. Different types of MP have different pollution sources. For example, PE and PP are widely used in ropes, fishing nets, agricultural plastic film materials, etc. [37]. These explanations support the PP density in our study. It has been reported that thermal power plants can produce over 10 million tons of fly ash and polypropylene wastes per year causing environmental pollution [38]. MP pollution was investigated in Mediterranean mussels (Mytilus galloprovincialis) sampled from 23 different stations in the Black Sea, Marmara Sea, and Aegean Sea coasts of Turkey, which are different environments compared to that of the present study. MP was detected in 48% of mussels, and the average MP presence was reported to be 0.69 pieces/mussels and 0.23 piece/g tissue. The morphological analysis of the latter study showed that MPs found in M. galloprovincialis were fragments (67.6%) > fibers (28.4%) > films (4.05%), and MPs with a size smaller than 0.5 mm were dominant, while the polymer type observed was PET (32.9%), PP (28.4%) and PE (19.4%) [39]. It is seen that the type, shape, and density of polymers in these studies are different from our study. In this case, the specific characteristics of the studied aquatic ecosystem and the species are considered to be behind this difference. However, in line with our results, Wakkaf et al. [40] reported that the most abundant MPs in mussels (M. galloprovincialis) were polypropylene and cellophane. Authors related this cohesion to the presence of settlements in the sampling zones.

4. Conclusions

The findings showed that Dreissena polymorpha of the stations of Beyhan reservoirs had high MP content. This result shows the first comprehensive evidence of MP pollution and its absorption and bioaccumulation in Dreissena polymorpha which is ecologically sensitive and collected from different points of Beyhan Dam Lake. With growing concerns about the MP contamination of aquatic ecosystems, more data on the fate and effects of MPs in these systems are needed to highlight research gaps and chart the future directions of studies on environmental MP pollution. While the study of the effects of MPs in freshwater including their presence, prevalence, characterization, and transport is particularly interesting, it is useful to evaluate potential solutions for MP pollution in these systems and provide multifaceted perspectives on this issue. Since MPs are now known to penetrate most, if not all, large ecosystems, the need to take measures to reduce environmental MP pollution seems to be a rapid necessity. The fact that the mussel species are not consumed as food does not reduce the importance of these studies.
Bioindicators especially the mussels play an important role in understanding pollution levels, bioavailability, and the ecological risks of pollutants. Although various bioindicators have been proposed to understand MPs in the marine environment, there are no bioindicators in the freshwater environments. The importance of the present study is the monitoring of MP pollution via zebra mussel D. polymorpha for the first time in this dam lake.
In summary, because of their ability to accumulate measurable amounts of pollutants, bivalve mollusks have often been chosen as environmental signaling transmitters (indicator or guard organisms). Among bivalves, the invasive zebra mussel (D. polymorpha), found in the Beyhan Dam Lake in Turkey, could be evaluated as a freshwater biological model for assessing the impact of microplastics.

Author Contributions

M.K., F.G., A.U. and V.P.: sampling, resources and formal analysis. D.A.: writing—review and editing. M.A.: conceptualization, writing—review and editing. G.A.: formal analysis, visualization, writing—original draft, writing—review and editing. 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 that support the findings of this study are available from the corresponding author upon reasonable request.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. The sampling stations in Beyhan Dam Lake, utilized from Google Earth.
Figure 1. The sampling stations in Beyhan Dam Lake, utilized from Google Earth.
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Figure 2. Dreissena polymorpha samples.
Figure 2. Dreissena polymorpha samples.
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Figure 3. Comparison of microplastic quantities in mussels at different stations in Beyhan Dam (n = 10, * p < 0.05).
Figure 3. Comparison of microplastic quantities in mussels at different stations in Beyhan Dam (n = 10, * p < 0.05).
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Figure 4. Color (A) and size (B) distributions of microplastics.
Figure 4. Color (A) and size (B) distributions of microplastics.
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Figure 5. Microplastic shape percentage (A) and microplastic microscope views (B) (a–c): fibers and (d–f): fragments. Scale: 0.3 mm.
Figure 5. Microplastic shape percentage (A) and microplastic microscope views (B) (a–c): fibers and (d–f): fragments. Scale: 0.3 mm.
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Figure 6. (A) FTIR spectrums of polymer types in mussel tissues, (B) percentage of polymer types.
Figure 6. (A) FTIR spectrums of polymer types in mussel tissues, (B) percentage of polymer types.
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Table
Table 1. Average length and tissue weight of D. polymorpha samples from 4 stations as well as the number of MPs observed per individual and number of MP observed per gram of mussel tissue (Mean ± SD) (n = 10, for each station).
Table 1. Average length and tissue weight of D. polymorpha samples from 4 stations as well as the number of MPs observed per individual and number of MP observed per gram of mussel tissue (Mean ± SD) (n = 10, for each station).
D. polymorphaLength (mm)Tissues Weight (g)MP/IndividualMP/gTotal MP
Station 1155.89 ± 6.220.63 ± 0.211.80 ± 0.923.47 ± 2.6218
Station 2154.84 ± 6.450.55 ± 0.191.60 ± 1.072.80 ± 2.1716
Station 3153.92 ± 7.300.53 ± 0.211.10 ± 0.742.41 ± 2.3111
Station 4154.16 ± 7.750.55 ± 0.240.70 ± 0.421.06 ± 0.977
Table
Table 2. Correlations between ∑MP and factors.
Table 2. Correlations between ∑MP and factors.
LengthTissue WeightMP/IndividualMP/g
Tissue weightPearson Correlation0.993 **
Sig. (2-tailed)0.000
N12
MP/individualPearson Correlation0.890 **0.895 **
Sig. (2-tailed)0.0000.000
N1212
MP/gPearson Correlation0.890 **0.895 **0.969 **
Sig. (2-tailed)0.0000.0000.000
N121212
Total MPPearson Correlation0.2960.3220.647 *0.569
Sig. (2-tailed)0.3510.3070.0230.053
* Correlation is significant at 0.05 level (2-tailed). ** Correlation is significant at 0.01 level (2-tailed).
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Atamanalp, M.; Kokturk, M.; Gündüz, F.; Parlak, V.; Ucar, A.; Alwazeer, D.; Alak, G. The Use of Zebra Mussel (Dreissena polymorpha) as a Sentinel Species for the Microplastic Pollution of Freshwater: The Case of Beyhan Dam Lake, Turkey. Sustainability 2023, 15, 1422. https://doi.org/10.3390/su15021422

AMA Style

Atamanalp M, Kokturk M, Gündüz F, Parlak V, Ucar A, Alwazeer D, Alak G. The Use of Zebra Mussel (Dreissena polymorpha) as a Sentinel Species for the Microplastic Pollution of Freshwater: The Case of Beyhan Dam Lake, Turkey. Sustainability. 2023; 15(2):1422. https://doi.org/10.3390/su15021422

Chicago/Turabian Style

Atamanalp, Muhammed, Mine Kokturk, Fatih Gündüz, Veysel Parlak, Arzu Ucar, Duried Alwazeer, and Gonca Alak. 2023. "The Use of Zebra Mussel (Dreissena polymorpha) as a Sentinel Species for the Microplastic Pollution of Freshwater: The Case of Beyhan Dam Lake, Turkey" Sustainability 15, no. 2: 1422. https://doi.org/10.3390/su15021422

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