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Article

Epiplastic Algal Communities on Different Types of Polymers in Freshwater Bodies: A Short-Term Experiment in Karst Lakes

by
Ekaterina Vodeneeva
1,2,*,
Yulia Pichugina
1,2,
Darja Zhurova
1,2,
Ekaterina Sharagina
1,
Pavel Kulizin
1,
Vyacheslav Zhikharev
1,
Alexander Okhapkin
1 and
Stanislav Ermakov
2,3
1
Institute of Biology and Biomedicine, Lobachevsky State University of Nizhny Novgorod, 23 Gagarin Av., 603022 Nizhny Novgorod, Russia
2
Institute of Applied Physics of the Russian Academy of Sciences, 46 Ulyanov St., 603950 Nizhny Novgorod, Russia
3
Institute of Shipbuilding and Water Transport Infrastructure, Volga State University of Water Transport, 5 Nesterova St., 603950 Nizhny Novgorod, Russia
*
Author to whom correspondence should be addressed.
Water 2024, 16(22), 3288; https://doi.org/10.3390/w16223288
Submission received: 21 October 2024 / Revised: 4 November 2024 / Accepted: 8 November 2024 / Published: 15 November 2024
(This article belongs to the Section Biodiversity and Functionality of Aquatic Ecosystems)
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Abstract

:
The increasing amount of plastic debris in water ecosystems provides a new substrate (epiplastic microhabitats) for aquatic organisms. The majority of research about epiplastic communities has focused on seawater environments, while research is still quite limited and scattered concerning freshwater systems. In this study, we analyze the first stages of colonization on different types of plastic by a periphytic algae community (its composition and dominant species complex) in freshwater bodies located in a nature reserve (within the Middle Volga Basin). A four-week-long incubation experiment on common plastic polymers (PET, LDPE, PP, and PS), both floating and dipped (~1 m), was conducted in two hydrologically connected karst water bodies in July 2023. The composition of periphytic algae was more diverse (due to the presence of planktonic, benthic, and periphytic species) than the phytoplankton composition found in the water column, being weakly similar to it (less than 30%). Significant taxonomic diversity and the dominant role of periphytic algae were noted for diatoms (up to 60% of the total composition), cyanobacteria (up to 35%), and green (including Charophyta) algae (up to 25%). The composition and structure of periphytic algae communities were distinct between habitats (biotope specificity) but not between the types of plastic, determined primarily by a local combination of factors. Statistically significant higher values of abundance and biomass were demonstrated for some species, particularly for Oedogonium on PP and Nitzschia on LDPE (p-value ≤ 0.05). As colonization progressed, the number of species, abundance, and dominance of individual taxa increased. In hydrologically connected habitats, different starts of colonization are possible, as well as different types of primary succession (initiated by potentially toxic planktonic cyanobacteria or benthic cyanobacteria and mobile raphid diatoms). Within the transparency zone, colonization was more active on the surface (for example, in relation to green algae on PP (p-value ≤ 0.05)). These results indicate a tendency for microalgae communities to colonize actively submerged plastic materials in freshwater, and they may be useful in assessing the ecological status of these aquatic ecosystems.

1. Introduction

Plastic pollution is considered a habitat hazard [1], posing a threat to both natural ecosystems and human health. According to data for 2021, the global volume of produced plastic amounted to 390.7 million tons [2], 80% of which was released into the environment. The negative impacts of plastic litter on the environment are well documented, including the chemical contamination of water [3], the fragmentation of “large” plastic particles, and the formation of microplastics (particles measuring 1–1000 μm [4] or 1–5000 μm [5] in size). Microplastics enter food chains [6,7,8], exerting a toxic effect on living organisms [9,10]. In addition, plastic debris can form a surface for the transfer of pollutants [11], pathogens and harmful species [12], or alien ones [13].
On the other hand, plastics act as substrates for the colonization of numerous aquatic organisms and promote the formation of bacterial, algal, and fungal fouling communities on their surfaces. The epiplastic community can change the properties of plastic [14], degrade plastic materials [15,16,17,18,19], and modify its flotation, causing the plastic to sink into the aphotic zone [20]. Biofouling can facilitate the colonization of plastic by macro-invertebrates, potentially serving as vectors for their dispersion [21,22,23].
This colonizing plastic community is termed the “plastisphere” [17]. Most research studies on plastisphere biota have focused on bacterial communities, ignoring or poorly considering the microalgae community in epiplastic complexes despite its fundamental role in a wide range of ecosystem functions [24].
The colonization of plastic particles is dependent on environmental conditions [25,26]; installation conditions (surface/bottom) [27,28,29]; or the size, topography, and roughness of the plastic substrate [27,30]. The initial colonization takes place in a few days or weeks, and its rate may depend on the types of plastic substrates [31]. In general, the first stages of the primary epiplastic community’s formation, despite the type of plastic, are similar. Over time, there is an increase in the total number of species and their abundance, as well as an increase in the dominance of some species [27,29,32].
Epiplastic algal communities stand apart in water bodies and have specific features with respect to their composition. [17,33,34,35,36]. It has been demonstrated that in all types of aquatic ecosystems, diatoms can be the most numerous, widespread, and diverse group of plastic colonizers [19,37,38], accounting for up to 60% of the total species number, while cyanobacteria accounted for 25%; other groups account for no more than 15% of species composition [31]. It is unclear and still an open question as to whether periphytic algae assemblages are typical for certain types of polymers. Some works [20,24,32] observed dissimilarities in algal community compositions based on distinct polymer substrates, or affinity appeared at a later date [28]. Others indicated the selectivity of some algae groups (for example, diatoms) in the colonization of particular polymer substrates [39].
Despite the ubiquity of plastic in the environment, the majority of research on the influence of plastic polymers on biofilm formation topics involves marine environments, whereas information about these events in freshwater ecosystems is still limited and should receive more scientific attention [29,32,40]. Such studies were conducted in, among others, reservoirs [29], wetland areas [32,41], rivers, and lakes [42].
Karst lakes have great importance among a variety of freshwater ecosystems. They play a crucial role not only in natural ecosystems but in human activities as well, providing a wide range of ecosystem services. Karst environments are under heavy human impact due to high tourist footfall and litter pollution, including that from plastic [43,44]. Such studies could be useful tools in providing information on the implications of plastic biofilms functioning on lake ecosystems and their response to pollution.
Here, we present a short-term in situ study with comprehensive analyses of the abundance and species composition of epiplastic algal communities, as well as their succession on different types of polymer materials in two connected karst freshwater bodies. Specifically, we focused on the following questions:
–
What is the similarity between the species composition of phytoplankton communities and communities of epiplastic algae, and is there any similarity between communities of periphytic algae on the same polymers within one water system?
–
Is there selectivity among microalgae taxa in colonizing the surfaces of certain types of plastic?
–
Are there differences in the initial stages of the colonization of epiplastic algal communities of different types of plastic?
–
Is there a difference in the periphytic algae community formation at different layers of the photic zone (surface and lower transparency limit)?

2. Materials and Methods

2.1. Study Area

The study was carried out on Lake Velikoye and in the channel (Protoka) connecting this lake with another one (Pustynsky Nature Reserve, Nizhny Novgorod region, Russia). It is located in the center of the Russian Plain on the northwestern edge of the Volga Upland, as part of the Teshe-Serezhinsky karst region. The karst of this territory is formed by both carbonates (limestones, dolomites, and marls) and sulfates (gypsum and anhydrite). The Serezha River, the third-order tributary of the Volga River (196 km length), flows through the territory of the Pustynsky Reserve. There are eight karst lakes in the reserve connected to a single system and representing the bays of the Serezha River. The catchment areas of these lakes are mainly forested.
Lake Velikoye is the upper lake in this system (Figure 1). The lake is oval in shape and elongated in the direction of the flow of the Serezha River (it flows into the east of the lake). The area of the lake is 91 hectares, with a length of up to 1600 m and width of up to 780 m. The average depth of the lake is 3.5 m, but in the center, there are depths of down to 11 m [45]. The lake has a eutrophic status [46]. The southern shore of the lake is low and represents a dimly defined floodplain of the Serezha River, and the northern shore is high. The bottom is muddy, whereas the shore zone is sandy and sandy–muddy.
Protoka is a channel connecting Lake Velikoye and Lake Svyato, and it is located on the right side of the Serezha River. It has an elongated shape, and its area is 25.31 hectares: length—1700 m; average width—60 m; average depth—1.8 m; maximum depth—3.5 m. During the summer period, homeothermic properties could be observed.

2.2. Experimental Design and Sampling

The plastic installations in this experiment were made up of ordinary plastics: mineral water bottles (polyethylene—PET), film (low-density polyethylene—LDPE), lunch boxes (polypropylene—PP), and floor insulation (polystyrene—PS). These types of plastic were chosen mainly because they are often found in freshwaters. Each installation contained one of four types of plastic, which were placed at two depths within the euphotic zone: on the surface and at the depth of 1 m. Surface sites were marked as “f” for floating sites, and underwater sites were marked “d” for dipped sites.
We previously prepared plastic materials before installing them in water. We sliced the edge of the plastic objects to make incisures of 5 × 5 cm on them so that it was easier to collect materials during the study period without damaging the entire plastic sample. Towards the end of the experiment, the particles of cut fragments became smaller due to force majeure, such as damage due to water flows, heavy rain, and probably tourists. However, we took this fact into account and recalculated the algae values for the new surface area. A total of eight types of epiplastic algal communities were examined: floating and dipped polyethylene (fPET and dPET, respectively), low-density polyethylene (fLDPE and dLDPE), polypropylene (fPP and dPP), and polystyrene (fPS and dPS).
The experimental setup was installed on 4 July 2023 at two littoral sites with open water surfaces (station 1—Protoka; station 2—Lake Velikoye (Figure 1)). The depth at the first station was 1.5 m, and at the second station, it was 2 m. Samples were collected 3, 10, 16, and 21 days after installation. Plastic fragments cut from the experimental substrates were placed in containers with lake water, which were immediately delivered to the laboratory. Also, 0.5-liter phytoplankton samples from the surface layer of the water body, as well as samples for water examination, were examined.
During the experiment, a large rainfall event was recorded from 8 July to 12 July (72 mm of precipitation fell in the study area, 11% of the annual norm). As a result, two dPS installations were not found in the 4th sampling (in both water bodies, on 20 July and 25 July). Thus, a total of 67 samples (phytoplankton and periphytic algae) were examined, and 5 samples were lost.

2.3. Environmental Parameters

Environmental parameters were recorded at each sampling station. Water transparency (SD, cm) was measured using a Secchi disk. The concentration of dissolved oxygen in the water (O2 % Sat), pH (pH), electrical conductivity (EC, μS/cm), and water temperature (WT, °C) were measured with multi-parameter hydrochemical probes ProODO and ProDSS (YSI Inc., Yellow Springs, OH, USA).
In the laboratory, the concentration of hydrocarbonates (HCO3−, mg/L) was determined titrimetrically in accordance with the standard method [47]. To determine the total phosphorus (TP) content, the samples were subjected to persulfate oxidation followed by the Morphy–Riley method [48]. The nitrite nitrogen (N-NO2) content in the sample was determined according to the Griess method, and nitrates (N-NO3) were determined via the photometric method using sodium salicylate [48,49]. The mass concentration of sulfate ions (SO42−, mg/L) was determined via the turbidimetric method proposed in a generally accepted manual [50]. The determination of dissolved forms of silicon (Si, mg/L) was based on the use of the colorimetry of the yellow silicon–molybdenum complex [48]. The turbidity value (TUF) was determined using the turbidimetric method [51]. The color of the samples was measured photometrically according to the chromium–cobalt scale [52].

2.4. Phytoplankton and Epiplastic Algal Community Analysis

Phytoplankton samples were concentrated using membrane filters (pore diameter 1.5–3.5 μm) to a volume of 5 mL in the laboratory. We examined 1–2 drops of the material in a living state, and the rest of the sample volume was fixed using iodine–formalin fixative.
Analysis of epiplastic algal communities was carried out according to the methods proposed by S. Komulainen [53]. Detailed laboratory measurements of the cut plastic fragments were carried out, and their area was calculated in accordance with the type of geometric figure (square or rectangle). The area of collected fragments ranged from 18 to 84.5 cm2. To determine the abundance and biomass of epiplastic algae, the fouling was brushed off and washed into a certain volume (5 mL) of filtered water from the studied water body. The samples were fixed with the iodine–formalin fixative.
Algae species identification was performed under a MEIJI Techno optical microscope (Saitama, Japan). The list of guides used for species identification was taken from the paper [54]. The current taxa names were verified using the AlgaeBase website [55]. Photos were taken with a Digital HDMI C-Mount camera ToupCam XCAMO720PHB. To avoid errors when identifying juvenile (sterile) stages of the green multicellular algae of different taxonomic groups (Chlorophyta and Charophyta) with a cortical thallus, we assigned these representatives to the group “Cortical multicellular green algae” (CMGA). In this group, we included genera such as Coleochaete (Charophyta), Protoderma, Phycopeltis, and Chaetophora (Chlorophyta), which were not able to form the features necessary for their identification during ontogenesis in a short-term experiment.
Information on the biotope preferences of the majority species was taken from [56]. We considered the next biotopic groups: planktonic—species (mobile and immobile) that drift in the water column (live mainly in the pelagic zone); littoral—species (mobile and immobile) that live mainly in the coastal zone; foulers—species that obligatorily inhabit submerged substrates (artificial and natural, including living organisms) and have adaptations for attachment (cortical thallus, rhizoids, mucous tubes, etc.); benthic—species that live on the ground; heterotopic—species that can change biotope (benthic-planktonic species, fouler-planktonic, etc.).
We analyzed phytoplankton abundance (N (106 cells/L)) and biomass (g/m3), as well as epiplastic algae abundance (N (103 cells/10 cm2)) and biomass (mg/10 cm2). The calculation of algae development indicators was carried out in a Nageotte counting chamber. The counting of large cortical forms of algae was carried out directly on plastic fragments under an inverted LOMO microscope (Russia).
The abundance of periphytic algae was calculated using the following formula:
N = ((AV0 × 40)/(V1nS)) × 10,
where A is the total number of counted cells, n is the number of calculated chamber stripes, V0 is the initial volume of the algae sample (mL), V1 is the volume of the test sample, and S is the surface of the plastic fragment.
Biomass (mg/10 cm2) was calculated using the volume-counting method in accordance with [53,57,58]. A detailed description of the calculation of the same indicators for the phytoplankton community is presented in the paper [59]. The dominant species included species with an abundance or biomass of more than 10% of the total value [60]. The trophic status of water bodies was determined based on the values of phytoplankton biomass in accordance with [61]: biomass < 1 g/m3—oligotrophic; 1–5 g/m3—mesotrophic; 5–10 g/m3—eutrophic; >10 g/m3—highly eutrophic.

2.5. Statistical Analysis

Taxonomical similarity between algal communities was assessed via pairwise comparison using the Sorensen (qualitative measure) indices (Ks) [62] according to the following formula:
Ks = 2 j/(a + b) × 100%,
where j is the number of common species in both water bodies, a is the number of species in reservoir A, and b is the number of species in reservoir B.
The data were clustered via Ward’s method, and the normalized Euclidean distance, expressed as a percentage ((Dlink/Dmax) × 100), was used as a metric.
The normality of the distribution of indicators of the quantitative development (abundance and biomass) of algal communities was assessed using the Shapiro–Wilk test. The homogeneity of the distribution of algae abundance and biomass was assessed using Levene’s test. Comparisons of the abundance and biomass of Oedogonium and Nitzschia in different types of plastic substrates were performed using the Kruskal–Wallis test. Comparisons of the total biomass, biomass, and abundance of green algae in PP polymers on the surface and in deep layers were performed using the Wilcoxon test. All analyses were performed using the open-source R software, version 4.4.2 (packages “vegan” and “statistics”) [63,64].

3. Results

3.1. Environmental Variables

We present the spectrum of environmental physical parameters at the sampling stations in Table 1. During the experiment, transparency in both water bodies ranged from 0.7 to 1.1 m, water temperature ranged from 17 to 27 degrees Celsius, and pH values ranged from 7.4 to 8.9. The oxygen saturation of water in Lake Velikoye varied in the range of 63.7–168.2%, and in Protoka, it ranged from 60.1 to 118.0%. Hydrocarbonate ions predominated in the composition of the water in both reservoirs, but their concentration in Lake Velikoye was significantly higher—up to 109.8 mg/L. Also, in Lake Velikoye, the specific conductivity values were higher from 97 to 128 μS/cm, while in Protoka, these values varied from 44 to 71 μS/cm. In Protoka, however, higher concentrations of sulfates were recorded (up to 0.3 mg/L), and water color values were also higher (119–160 degrees on the chromium–cobalt scale). The silicon content in the water of the studied reservoirs was similar. The concentration of TP was higher in Lake Velikoye (varied there from 13.5 to 19.9 μg/L), while the nitrate nitrogen (N-NO3) content was higher in Protoka. The nitrite nitrogen (N-NO2) content was the same in both water bodies.
After the rainfall event, on 14 July, a decrease in temperature, electrical conductivity, and the amount of bicarbonates and a decrease in oxygen concentration were recorded in both reservoirs. An increase in water color was also noted in Lake Velikoye.

3.2. Taxonomical and Ecological Composition of Phytoplankton and Periphytic Algae of Different Plastic Substrates

The phytoplankton of Lake Velikoye was formed by 45 taxa, and in Protoka, it was formed by 34 taxa; all of them belong to 6 taxonomical groups (Table S1). The species list in both reservoirs was dominated by green algae (31–37% of the total composition) and cyanobacteria (25–31%), whereas diatoms were also noticeable (18%) in Lake Velikoye.
The species composition of periphytic algae was noticeably richer than the composition of local phytoplankton and included more than 140 taxa. The total number of periphytic algae species in Lake Velikoye was 116, while in Protoka, it was 63. The maximum number of algae species was observed on polyethylene terephthalate (PET) in both Lake Velikoye (81 taxa) and Protoka (47 taxa); the minimum was observed on polystyrene (PS). Algal biofilms were mostly composed of diatom species (up to 60% of the total species composition of epiplastic algae), cyanobacteria (up to 35%), and groups of green algae (Chlorophyta and Charophyta—up to 25%).
The phytoplankton composition in Lake Velikoye was formed by planktonic species (60–80%) (Figure 2). In the first days of colonization, the predominance of planktonic species remained on all types of plastics installed in the lake, but from the tenth successional day, the proportion of benthic and littoral forms gradually increased, while the proportion of planktonic species remained at the level of 18–50%. In Protoka, as well as in Lake Velikoye, the planktonic forms prevailed (more than 50%) (Figure 3). On plastic substrates, during the initial colonization stage, the heterotopic species predominated; later, benthic and foulers predominated while the proportion of planktonic species did not exceed 10–30%.
Similarity in the composition of planktonic algae and periphytic algae was low: in Lake Velikoye. The similarity coefficient varied from 7 to 34%, and in Protoka, it varied from 0 to 15% (Figure 4). We also found a weak similarity in the composition of periphytic algae colonizing identical polymers submerged in different water bodies. The composition similarity of periphytic algae relative to PET in Lake Velikoye and Protoka, as well as PS in these reservoirs, was 23–24%. The species composition of the LDPE and PP fouling organisms of these water bodies was similar by 32%. Data visualization (Figure 5) clearly showed the separation of aquatic ecosystems according to the composition of periphytic algae, although there was an insignificant degree of commonality. In Protoka, we noted a greater grouping of data, indicating greater commonality in the composition of fouling organisms during the 20-day experiment, in contrast to Lake Velikoye. Obligatory fouling organisms in this water body initiated the colonization of plastics, while in Lake Velikoye, an allochthonous community composed of plankton species was first formed (data for 7 July).
A dendrogram was constructed based on the generalized similarity matrix (using the Sørensen coefficient) of the species composition of phytoplankton and periphytic algae. In the first days of exposure (Figure 5), the composition of periphytic algae was close to the composition of phytoplankton (cluster 1). This cluster has several subgroups. Two of them (1a and 1b) combine planktonic samples of algae that float in the water column and do not colonize plastic substrates at the study time. Moreover, phytoplankton samples from Lake Velikoye and Protoka were clustered in different groups. The last subgroup (1c) clustered primary substrate colonization samples (7–14 July). This group had the closest connection with samples of phytoplankton from Lake Velikoye.
Other groups (cluster 2 and 3) were formed by assemblages of periphytic algae referring to the 10th, 16th, and 21st days of succession. However, the composition of algae of the same plastic substrates in two water bodies differed (cluster 2 (Velikoye) and cluster 3 (Protoka)).

3.3. Abundance and Biomass of Phytoplankton and Periphytic Algae Communities of Different Plastic Substrates

During the experiment, cyanobacteria predominated in the phytoplankton of Lake Velikoye, forming 86–99% of the total abundance and 11–93% of the total biomass. Sometimes, dinoflagellates prevailed (84%) (Figure 6 and Figure 7). The average values of phytoplankton abundance were 30.09 ± 18.08 million cells/L; for biomass, it was 3.71 ± 2.19 g/m3 (maximum biomass—more than 10 g/m3). Based on these values, the lake was classified as mesotrophic–eutrophic.
The phytoplankton of the Protoka was dominated by different groups. At the beginning of July, green algae predominated in abundance (56–84% of the total indicators), and raphidophyte algae (Ochrophyta) predominated as well—22–34% (Figure 8). The last group was most noticeable with respect to biomass—up to 90–100% (Figure 9). Subsequently, the role of green algae decreased, and the proportion of cyanobacteria increased. The average values of the abundance (1.11 ± 0.41 million cells/L) and biomass (3.09 ± 1.24 g/m3) of phytoplankton characterized Protoka as mesotrophic.
The colonization of all plastic substrates in Lake Velikoye began on the third day of the experiment. However, in Protoka, on the third day, PP and PS (both horizons) and LDPE (surface) remained uninhabited. The photo timeline of the plastic substrates’ colonization is presented in Figure 10.
The maximum periphytic algae abundance in both water bodies was observed on PP and PET substrates installed on the surface—5.6 × 106 cells/10 cm2 and 3.4 × 106 cells/10 cm2 (Lake Velikoye) and 0.7 × 106 and 0.4 × 106 cells/10 cm2 (Protoka), respectively (see Figure 11). The highest biomass values were also noted for surface samples—PET (917 mg/10 cm2) and PP (2481) in Lake Velikoye; PET (314) and PS (396) in Protoka.
The abundance and biomass dynamics of periphytic algae on all types of plastic installed on the surface were similar in both water bodies and were characterized by a noticeable increase in values (Figure 11). At a depth of 1 m, the algae abundance developed in a different way. Thus, in Lake Velikoye, with respect to substrates PET and LDPE, with the exception of PS (due to the material loss, it was not possible to assess these events), on the twentieth day of the experiment after growth, a decrease in abundance and biomass was noted. Perhaps heavy rainfall and cooling (Figure 11) contributed to a slowdown in the rate of colonization, as well as in the growth rate of adhered species.
In Lake Velikoye, during the first stage of epiplastic algal community formation, cyanobacteria planktonic species predominated (97% of the total number and 95% of the biomass) on floating LDPE substrates, as well as in phytoplankton communities (Figure 6 and Figure 7). The abundance prevalence of this group species was also noted on PP and PS polymers; however, the biomass for these substrates was determined by unicellular green algae (up to 63% of the total value) and centric diatoms (up to 73%). In the deep layers, the role of diatoms as substrate foulers increased. Diatoms prevailed both in abundance and in biomass, especially in PP (up to 77–98% of total). On the floating PET substrate, colonization by cyanobacteria was not observed in the first days—green algae, diatoms, and dinoflagellates dominated here. For the dipped PET samples, cyanobacteria dominated by abundance (up to 50% total); diatoms and dinophytes dominated by biomass. Within 10 days, raphid pennate diatoms and filamentous green algae began to predominate on the floating LDPE and PP, and cyanobacteria began to predominate on the fPET. Starting from 20 July, active colonization by cortic green algae was observed with respect to fPET, fLDPE, and fPP, with 80–90% proportions in terms of abundance and biomass. At a depth of 1 m, these algae only colonized dPP substrates. As for the dipped LDPE and PET substrates, they were colonized by pennate diatoms, filamentous green algae, and ochrophytes, whereas dPS plastics were colonized by cyanobacteria and filamentous green algae.
In Protoka, only the PET substrates were colonized by algae (raphid diatoms) after three days both on the surface and at the depth layer (Figure 8 and Figure 9). Within 10 days, on floating PETs, cyanobacteria (50% of total) and filamentous green algae began to dominate in abundance, and raphid diatoms (60–70%) began to dominate by biomass. In subsequent days, dominance on fPET changed for CMGA (70–80% of total). On dPET, the benthic species of cyanobacteria dominated in abundance, whereas green filamentous algae dominated by biomass. Another type of succession was observed on the LDPE substrate. This polymer was mainly colonized by cyanobacteria (up to 47–90% of total abundance) and represented firstly by planktonic species; then, it was represented by bentic ones. This group had a significant role in the algal community biomass only at the beginning of the experiment; then, raphid diatoms started to dominate (up to 60–90%). The PP and PS substrates were colonized by green algae (including CGMA forms) diatoms and cyanobacteria. On floating polystyrene, green filamentous algae (up to 80–95% of total) and diatoms dominated in abundance; the last group was more noticeable (70% of total) on the submerged substrates. In the first two weeks, the floating polypropylene was colonized by green algae (45%), cyanobacteria (35%), and diatoms (18%) in fairly equal proportions. At different depths, the plastic was colonized by cyanobacteria or green algae and diatoms. In the final stage, a clear difference between installation substrates was noted: CMGA started to dominate on the surface, and benthic cyanobacteria started to dominate at the dipped layer.
In both reservoirs, with increasing exposure time, the number and biomass of algae on plastic substrates also increased. The abundance and biomass of periphytic algae were higher for the surface installations, sometimes exceeding those on the dipped supports more than 100 times. However, despite such sharp differences, only the abundance and biomass of green-algae-colonizing floating PP plastic, as well as the values of the total biomass, turned out to be statistically different (Figure 12).

3.4. Dominant Species of Phytoplankton and Periphytic Algae Communities in Different Plastic Substrates

The dominant species in the phytoplankton of Lake Velikoye were filamentous cyanobacteria—Aphanizomenon flos-aquae Ralfs ex Bornet & Flahault (up to 90% of the total values)—and Dolichospermum species—up to 10–15% of the total values (Figure 13). Among the biomass-dominant species, there were dinophyte algae Ceratium cf. hirundinella (O.F.Müller) Dujardin and Peridinium species. In the phytoplankton of Protoka, the main dominant species was a representative of raphidophytes—Gonyostomum semen (Ehrenberg) Diesing (Figure 13). Its abundance contribution ranged from 22 to 35%, and the biomass contribution was up to 95%. Among green algae, small-celled coccoid species Lemmermannia triangularis (Chodat) C.Bock & Krienitz was noticeablye in abundance.
The list of dominant periphytic algae species in polymer substrates and their dominance frequency are presented in Table 2.
Figure 14 shows some dominant species among periphytic algae. In the group of cyanobacteria, Aphanizomenon flos-aque was found in all types of plastic and in almost all installations, and it was dominant in local phytoplankton. A high dominance frequency for this species was noted in dLDPE. Among other cyanobacteria, the species of the genus Pseudanabaena was dominant in terms of abundance in all types of polymeric materials, and the benthic species of the genus Oscillatoria was dominant in terms of biomass. Phormidium was noted to be frequently dominant.
Among the diatoms, pennate taxa such as Navicula were found on all polymers and were biomass-dominant (13–75% of the total values), and Gomphonema, Eunotia, Pinnularia, and Tabellaria fenestrata (Figure 14) were also observed. The last species was found on floating and dipped PET polymers, as well as on fPP and fLDPE with high occurrences—75% of all samples. Among the centric diatoms, Cyclotella sp. is noted on all types of polymer substrates, and it is mainly biomass-dominant.
Among the dominant green algae, the highest occurrence was noted for Oedogonium (on PS—43 and 50% in abundance and biomass, respectively; on PET—38 and 25%). On almost all types of plastic (except PS), green cortical algae (Coleochaete (Charophyta), Protoderma, Phycopeltis, and Chaetophora (Chlorophyta)) were among the dominants. A high occurrence of these algae as dominants (in half of the cases) was noted for PP and PET. Statistically significant higher values of abundance were demonstrated for Oedogonium on polystyrene, and higher abundance and biomass values were demonstrated for Nitzschia (diatoms) on LDPE (Figure 15).
Dominant taxa from other groups (Ochrophyta (Xanthophyceae, Raphidophyceae), Dinophyta, and Euglenophyta) were presented both by a smaller number of species and by their role in the community.

4. Discussion

Based on the ion content, both studied reservoirs belong to the hydrocarbonate type [65]. Despite the hydrological connection, the waters in the Protoka were more humic [66], with higher water color values and lower pH and conductivity compared to Lake Velikoye. Coniferous and mixed forests were presented within the catchment area of Protoka, removing humus from it, coloring the water, and decreasing mineralization. Higher concentrations of TP in Lake Velikoye contributed to the phytoplankton biomass at the mesotrophic–eutrophic level.
The results obtained in this work demonstrate that plastic surfaces may host various species of microalgae from different taxonomical groups in freshwater lakes. This is similar to other studies indicating that plastic surfaces provide new niches in the aquatic environment available for colonization by a wide range of organisms (biofouling) [17,67,68,69]. During the experiment, we established that the species composition of periphytic algae is richer (more than three times) than the composition of local phytoplankton due to both planktonic and benthic species that took part in the colonization of polymer materials. The same increasing patterns with respect to the proportion of non-planktonic forms on plastic substrates during the exposure period were demonstrated in other works [27,70].
It has been widely reported that the algal community growing on plastic debris is consistently different from the surrounding free-living phytoplankton species [17,33,34,35,36,71]. The same result was obtained in our 4-week exposure—the dissimilarity between phytoplankton and periphytic algae communities was more than 70–80% divergence.
The composition of the algae fouling of the same plastic materials submerged in two water bodies was also different despite their hydrological connection. This was confirmed by the low values of the Sørensen index (less than 30%), as well as by the results of cluster analysis.
We found that plastic polymers did not have a significant influence on biofilm development. The formation of the taxonomic diversity of the epiplastic algal community was mainly determined by a local combination of abiotic and biotic factors. The importance of local conditions as predictors of the composition of plastisphere communities has been indicated in the natural environment for both marine [72] and freshwater ecosystems. For example, such patterns were revealed during the analysis of microplastonic LDPE films in hydrologically different freshwater reservoirs, where the “biotope-specific” patterns of the species composition and the spatial structures of fouling communities were noted during initial colonization [42]. Similar results were demonstrated when setting up an experiment with immersed plastic in mesocosms [24]. Nutrient concentration, temperature, light, grazing, and habitat heterogeneity and hydrological events seem to be the most crucial factors in the sorting of algae species in the plastisphere community [25].
The formation of an autochthonous periphytic algal community on artificial substrates was similar in both reservoirs; it started on the 10th day of exposure (14 July). The first stages of succession that we identified were generally consistent with the following three classic phases of bacterial biofilm development in all types of substrates (artificial and natural): primary colonization after 3 days; growth phase after 10 days; maturation phase after 30 days [73]. Apparently, the changes that occur for any substrate during the period of active bacterial growth create conditions for their colonization by true algal foulers. Similar terms (9–15th succession days) for the separation of periphytic algae communities were noted in the Rosana Reservoir (Corvo Stream, Parana State, Brazil). This research provided an analysis of the heterogeneity of communities on artificial and natural substrates that are under the influence of colonization time [74]. Therefore, it can be assumed that the formation periods of these communities are similar in different types of water bodies and on different substrates.
Diatoms, cyanobacteria, and green algae are considered the first microorganisms to colonize plastic waste [69], and they determine the diversity of the periphytic algae community [19,27,32,37,38]. We also noted that the predominant group in terms of diversity in plastic fouling was diatoms (up to 60% of the total species composition of epiplastic algae), and the second and third positions were occupied by cyanobacteria (up to 35%) and green (including Charophyta) algae (up to 25%). These taxa not only determined diversity but also had a dominant role in plastisphere algal communities.
Diatoms are considered common and omnipresent residents of the plastisphere [71,75]. Pennate diatoms are capable of firmly attaching to plastic and resisting water turbulence and wave action [19]. Diatoms are capable of creating specific architecture on the surfaces [33,42], as they can grow both flat on the surface of plastic materials and form vertical colonies attached to mucous pads [19]. The presence of diatoms can be observed in up to 100% of collected plastic waste samples. In our studies, diatoms made up more than half of the total composition of fouling organisms and turned out to be the most diverse group among the dominants.
Common diatoms reported in previous plastisphere research include species belonging, for instance, to genera Achnantes, Amphora, Cocconeis, Navicula, and Nitzschia [24], which were all observed in our study (Table 2). The genus Navicula, which has the highest occurrence, is a very common taxon and is widely observed in plastic waste in aquatic systems [24,32].
It is known that diatoms are among the first recruits during the colonization of different substrata and after the formation of the ‘conditioning layer’ on the surface by bacteria; they are also capable of initiating colonization independently by attaching to the virgin surface [24]. Diatoms represent a fundamental step in biofouling, influencing the subsequent colonization process [76]. In our experiment within one lake system, we observed different variants with respect to the colonization of plastic substrates. In Lake Velikoye, the first stages of colonization were performed by cyanobacteria planktonic species, especially on floating supports. In Protoka, the colonization of the same polymers (particularly, PET) was initiated by diatoms.
Cyanobacteria, along with diatoms, play an important role in plastic colonization. Due to their ecological plasticity, these organisms are able to adapt to various environmental conditions; therefore, they are often observed in plastisphere communities [24], providing important processes in biofilms [71]. Among cyanobacteria, the most frequent residents of the epiplastic algal community are filamentous species of the genera Phormidium and Oscillatoria, which are widespread and abundant in marine plastic debris [17,27,71,77,78] and freshwater ecosystems [42]. As for coccoid ones, the genera Microcystis, Synechococcus, Aphanocapsa, etc., were noted [24]. We also observed Phormidium and Oscillatoria among the dominant species, but the highest occurrence was noted for another filamentous cyanobacteria species Aphanizomenon flos-aquae, in complex with the Dolichospermum species predominating in plankton during this period. Some cyanobacteria are known to contribute to plastic degradation [79]; for example, filamentous cyanobacteria Phormidium degrade hydrocarbons [76]. In a study of mangrove ecosystems [80], it was shown that degradation was obviously evident in the treatment of LD polyethylene sheets using the filamentous microalgae Anabaena spiroides, having a high percentage of decomposition (18%). On the other hand, some cyanobacteria species are capable of producing cyanotoxins, so the accumulation of these organisms on plastic waste in water bodies can have harmful consequences for the ecosystem.
The subsequent stage of colonization on most plastic substrates was the development of branching cortical thalli of green algae (in a broad sense, including Chlorophyta and Charophyta taxa), the generic and species identification of which was difficult due to their juvenile stage. Some representatives are obligate foulers of various submerged substrates and prefer to colonize flat areas of the surface [42,78]. The morphology of the thallus of these algae, as well as the way they grow, promotes the adhesion of thallus cells with polymers, which provides advantages in further stages of colonization. Among fouling organisms from green algae, filamentous genus Oedogonium, which has special structures for attachment to the substrate, was an active settler of plastic. The presence of coccoid forms of green algae, as well as unicellular representatives of other groups (Xanthophyceae, Raphidophyceae, Dinophyceae, and Euglenophyceae), was noted sporadically, representing the result of stochastic processes that determine the presence of some species on different substrates, which is no exception [24].
Among the controversial issues of the topic of plastic fouling is the question of whether there is a relationship between the type of plastics and the species that colonize them. Some studies have demonstrated the selective colonization of certain types of plastic by algae when compared with inert control materials or when comparing different types of plastics. In particular, Dudek et al. [39] demonstrated that the diatom Mastogloia corsicana by the end of a 6-week incubation period predominantly colonized the PP polymer, and Striatella sp. colonized PET. However, such selectivity was not noted in other studies [24,42]. We also did not mark any dependence of microalgae species in the colonization of different polymers. Apparently, it is the pool of local species and not the polymer type that is the determining factor in the formation of the epiplastic algal community. This pattern has been observed both in studies of periphyton assemblages in temperate lakes (many algae species identified in periphyton were common components of the phytoplankton community) [81] and in experiments in mesocosms [24,82]. For some taxa, we noted statistically higher values with respect to their abundance and biomass (in particular, for Oedogonium on PS and Nitzschia on LDPE (Figure 15)). However, taking into account that polymeric materials can differ in chemical characteristics and the presence of various additives [67], the obtained results should be interpreted with caution and require clarification. On the other hand, physical plastic properties such as hydrophobicity and surface roughness may also provide microhabitats and shelter, facilitating microalgae attachment and colonization [83]. This was noted in relation to diatom species, whose abundance increased in plastics with a rough surface [84,85]. To obtain more reliable results, our findings must be examined in many interactions, which we have planned for the future.
It is known that the rate of plastic substrate colonization can vary [29]. Our experiment showed that when comparing two water bodies, colonization was more active in Lake Velikoye; here, it began for all types of polymer materials from the third day of exposure. In Protoka, on the third day, PP and PS (both installations) and LDPE (surface) remained uninhabited. Perhaps the reason was the low concentration of planktonic cyanobacteria there that are capable of secreting mucus, contributing to the primary degradation of plastic and the formation of conditions for the settlement of other species [71,78]. Another possible reason could be the lower light conditions in Protoka due to the increased water color values.
The first stages of succession generally coincided with those already noted earlier for other water bodies: There is an increase over time in the total number of species and the abundance, as well as an increase in the dominance of individual representatives [27,29,32]. In both reservoirs, with increasing colonization times, the abundance and biomass of periphytic algae also increased, especially for surface installations. Differences between dipped and floating supports can be attributed to the surface supports having a higher light intensity and being more exposed to phenomena that promote transport, adhesion, and nutrient exchange [32].
Extending the exposure time will allow us to analyze the structure of mature communities and expand our understanding of the patterns of periphytic algae formation. For example, Smith et al. [29], when studying the formation of plastisphere communities over time, revealed significant differences between diatom communities after 4 or more weeks. An important factor in a community’s formation is also the artificial and natural submerged substrates located near the installation site, which potentially contain an inoculum of settlers. For example, various macrophytes can provide a source of microalgae species that subsequently form a biofilm [86].
The outcomes of this study provide valuable contributions that fill the lack of knowledge about the peculiarities of algal biofilm formation on plastic polymers in freshwater. To the best of our knowledge, this is the first in situ field experiment devoted to the comparative analysis of the initial stages of the periphytic algae community’s formation in common types of plastic polymers (PET, LDPE, PP, and PS) in a hydrologically connected system of karst water bodies in a natural reserve with strong anthropogenic impact. In further studies, we plan to take into account a larger set of factors for a more complete understanding of the stages of biofilm formation, and we aim to increase the number of experimental replicates.

5. Conclusions

The results of this study demonstrated the tendency for the formation of periphytic algae (increasing diversity, abundance, predominance, and preference for surface), which are generally similar to those noted in other freshwater and marine ecosystems. The weak similarity between periphytic algae and phytoplankton, as well as between the epiplastic algae of the same polymers in different water bodies, indicates the biotope specificity of periphytic algae formation. Local species composition and local factors turn out to be more important than the type of polymers in controlled species sorting. At the early stages of colonization, biotope heterogeneity can also determine the adhesion start time of algal substrates, as well as the various paths of primary succession, including the participation of potentially toxic cyanobacteria.
This research has environmental significance for understanding the functioning of water bodies. First of all, this study provides clarification on the relative role of plastic fouling communities in biogeochemical cycles and aquatic food chains in freshwater ecosystems, and it more accurately determines their trophic capacity. Another important aspect is the ability of plastic with biofilms to act as a vector for the dispersal of various living organisms, including toxic, pathogenic, and invasive species, which is especially important in water bodies with high anthropogenic impact. These issues need further investigation.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/w16223288/s1. Table S1: List of algae species recorded in the studied water bodies during the experimental period.

Author Contributions

Conceptualization, methodology, and writing—original draft preparation, E.V.; data curation and investigation, Y.P. and D.Z.; visualization, P.K. and E.S.; formal analysis, V.Z.; supervision and writing—reviewing and editing, A.O.; project administration, S.E. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Russian Science Foundation: grant number 23-17-00167.

Data Availability Statement

Data is contained within the article.

Acknowledgments

The authors express their sincere gratitude to V.A. Dobrokhotov, T.N. Lazareva, and G.V. Leshchev (Institute of Applied Physics of the Russian Academy of Sciences) for their assistance in fieldwork.

Conflicts of Interest

The authors declare no conflicts of interest.

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Water 16 03288 g001
Figure 1. Location of study area.
Figure 1. Location of study area.
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Figure 2. Ratio (%) of biotopic groups of phytoplankton and periphytic algae communities in plastic substrates in Lake Velikoye.
Figure 2. Ratio (%) of biotopic groups of phytoplankton and periphytic algae communities in plastic substrates in Lake Velikoye.
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Water 16 03288 g003
Figure 3. Ratio (%) of biotopic groups of phytoplankton and periphytic algae communities in plastic substrates in Protoka.
Figure 3. Ratio (%) of biotopic groups of phytoplankton and periphytic algae communities in plastic substrates in Protoka.
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Water 16 03288 g004
Figure 4. Similarity matrix (%) of the species composition of plankton algae and periphytic algae of different plastic substrates during the study period (V—Lake Velikoye; P—Protoka) (A). Visualization of the species’s composition similarity of periphytic algae (B).
Figure 4. Similarity matrix (%) of the species composition of plankton algae and periphytic algae of different plastic substrates during the study period (V—Lake Velikoye; P—Protoka) (A). Visualization of the species’s composition similarity of periphytic algae (B).
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Figure 5. Dendrogram of the dissimilarity in the species composition of phytoplankton and periphytic algae on different types of plastic.
Figure 5. Dendrogram of the dissimilarity in the species composition of phytoplankton and periphytic algae on different types of plastic.
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Water 16 03288 g006
Figure 6. The ratio (%) of algae phyla in the abundance of phytoplankton and epiplastic algal communities in Lake Velikoye.
Figure 6. The ratio (%) of algae phyla in the abundance of phytoplankton and epiplastic algal communities in Lake Velikoye.
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Water 16 03288 g007
Figure 7. The ratio (%) of algae phyla in the biomass of phytoplankton and epiplastic algal communities in Lake Velikoye.
Figure 7. The ratio (%) of algae phyla in the biomass of phytoplankton and epiplastic algal communities in Lake Velikoye.
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Water 16 03288 g008
Figure 8. The ratio (%) of algae phyla in the abundance of phytoplankton and epiplastic algal communities in Protoka.
Figure 8. The ratio (%) of algae phyla in the abundance of phytoplankton and epiplastic algal communities in Protoka.
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Water 16 03288 g009
Figure 9. The ratio (%) of algae phyla in the biomass of phytoplankton and epiplastic algal communities in Protoka.
Figure 9. The ratio (%) of algae phyla in the biomass of phytoplankton and epiplastic algal communities in Protoka.
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Water 16 03288 g010
Figure 10. Photos of the fouling of different plastic substrates exposed on the surface (A) and 1 m deep (B) (horizon 1a, 1b—7 July; 2a, 2b—14 July; 3a, 3b—20 July; 4a, 4b—25 July).
Figure 10. Photos of the fouling of different plastic substrates exposed on the surface (A) and 1 m deep (B) (horizon 1a, 1b—7 July; 2a, 2b—14 July; 3a, 3b—20 July; 4a, 4b—25 July).
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Figure 11. Dynamics of the abundance and biomass of periphytic algae on different types of plastic installed in the surface layer and at a depth of 1 m in Lake Velikoye (A,B) and Protoka (C,D). Precipitation (mm) and air temperature (E) (https://nuipogoda.ru/).
Figure 11. Dynamics of the abundance and biomass of periphytic algae on different types of plastic installed in the surface layer and at a depth of 1 m in Lake Velikoye (A,B) and Protoka (C,D). Precipitation (mm) and air temperature (E) (https://nuipogoda.ru/).
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Water 16 03288 g012
Figure 12. Total biomass (A) and the abundance and biomass of green algae ((B) and (C), respectively) in PP polymer fouling on the surface and in deep layers.
Figure 12. Total biomass (A) and the abundance and biomass of green algae ((B) and (C), respectively) in PP polymer fouling on the surface and in deep layers.
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Figure 13. Dominant species of cyanobacteria and algae in phytoplankton (scale bar is 10 µm): (A)—Aphanizomenon flos-aquae; (B)—Ceratium cf. hirundinella; (C)—Dolichospermum spiroides; (D–F,I)—Dolichospermum spp.; (H)—Pseudanabaena sp.; (G)—Gonyostomum semen.
Figure 13. Dominant species of cyanobacteria and algae in phytoplankton (scale bar is 10 µm): (A)—Aphanizomenon flos-aquae; (B)—Ceratium cf. hirundinella; (C)—Dolichospermum spiroides; (D–F,I)—Dolichospermum spp.; (H)—Pseudanabaena sp.; (G)—Gonyostomum semen.
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Figure 14. Dominant species of periphytic algae communities of different plastic substrates (scale bar is 10 mkm): (A,B)—CMGA ((A)—cf. Coleochaetae; (B)—cf. Chaetophora); (C)—Oedogonium sp.; (D)—Oscillatoria sp.; (E)—Tabellaria fenestarata; (F)—Navicula radiosa; (G,H)—Gomphonema capitatum.
Figure 14. Dominant species of periphytic algae communities of different plastic substrates (scale bar is 10 mkm): (A,B)—CMGA ((A)—cf. Coleochaetae; (B)—cf. Chaetophora); (C)—Oedogonium sp.; (D)—Oscillatoria sp.; (E)—Tabellaria fenestarata; (F)—Navicula radiosa; (G,H)—Gomphonema capitatum.
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Figure 15. Average values of Oedogonium abundance (A) and Nitzschia abundance and biomass ((B) and (C), respectively) in different types of polymers.
Figure 15. Average values of Oedogonium abundance (A) and Nitzschia abundance and biomass ((B) and (C), respectively) in different types of polymers.
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Table 1. Some limnological parameters of water bodies during the study period.
Table 1. Some limnological parameters of water bodies during the study period.
Variables Protoka Lake Velikoye
4 July7 July14 July 20 July 25 July 4 July7 July 14 July 20 July 25 July
Transparency, cm110110707070100100707070
WT, °C22.5924.816.9620.06−26.5226.9617.1819.75−
EC, μS/cm51.8646.7144.2371.34−128.65128.9797.94110.52−
O2, % Sat113.68109.0670.3696.14−131.64166.4875.8498.61−
pH8.097.567.458.92−8.598.597.817.65−
Si, mg/L−0.891.151.372.49−0.700.981.853.33
SO42−, mg/L−0.070.110.040.31−0.010.040.010.04
HCO3−, mg/L−27.456.8630.5027.45−109.8313.7241.1813.72
TP, μg/L−6.754.3010.4414.12−13.5116.8919.6519.96
N-NO2, μg/L−3.163.193.023.02−3.083.233.122.98
N-NO3, mg/L−0.760.630.381.12−0.170.490.710.52
TUF−0.420.080.420.01−0.800.010.280.46
Color, °−156119127160−6576133158
Table 2. Frequency of dominance (%) in the abundance- and biomass-dominant taxa (indicated in parenthesis) of cyanobacteria and algae in the epiplastic algal community.
Table 2. Frequency of dominance (%) in the abundance- and biomass-dominant taxa (indicated in parenthesis) of cyanobacteria and algae in the epiplastic algal community.
Dominant TaxafPETdPETfLDPEdLDPEfPPdPPfPSdPS
Cyanobacteria
Aphanizomenon flos-aquae1212−50 (12)12121225
Aphanocapsa incerta−12−12 −−−−
Dolichospermum spp.−−25 (12)25 (12)−−−−
Lyngbya spp.−−−(12)12−29 (25)−
Merismopedia spp.−−−12−−−−
Oscillatoria spp.−−25 (12)(12)−25 (12)−(13)
Phormidium spp.−25 (25)2525−(12)−−
Pseudanabaena spp.1212−251225−25
Green algae (Chlorophyta + Charophyta)
CMGA *50 (50)−25 (25)−38 (38)12−−
Chlorophyta
Bulbochaete sp.−−−−−(12)−−
Coenococcus planctonicus12−−−−12−−
Coenochloris fottii−−−−−12−(13)
Crucigenia quadrata−−−−12−−−
Dictyosphaerium pulchellum−12−−−−−−
Oedogonium spp.38 (25)12 (25)12(25)25 (25)12 (25)43 (50)−
Pediastrum duplex−−−−12(12)−−−
Bacillariophyta
Aulacoseira granulata−−−−−12(12)−−
Amphora ovalis−−−−−−(12)−
Cyclotella spp.(12)25 (38)(12)12(12)−−−
Cymbella spp.−−(38)(12)−−−−
Eunotia sp.(12)(12)−(25)−−−−
Fragilaria sp.−−−(12)(12)−−−
Gomphonema sp.(12)(25)−−−−−−
Lindavia comta1212(12)−−12−25
Melosira varians−12 (12)12−−(12)−−
Navicula spp.(12)(25)(38)(63)12 (25)38 (75)(12)(12)
Nitzschia spp.12 (12)−−(12)−12 (12)−−
Pinnularia sp.−(25)−−(12)(12)−−
Stephanodiscus spp.−−−12 (12)−25−−
Tabellaria fenestrata12 (12)25 (38) 25(38)−25(12)−−
Ulnaria ulna−(12)−−(12)−−−
Ochrophyta (Xanthophyceae)
Tribonema spp.−−−25 (25)−(12)(12)−
Ochrophyta (Raphidophyceae)
Gonyostmum semen−−−−−(12)−−
Dinophyta
Ceratium cf. hirundinella(12) −−−−−−−
Gymnodinium sp.−−(12)−−−−−
Peridinium spp.12 (12)12 (12)(12)−−−−−
Euglenophyta
Phacus sp.−−−−−(12)−−
Note: * CMGA—cortical multicellular green algae.
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Vodeneeva, E.; Pichugina, Y.; Zhurova, D.; Sharagina, E.; Kulizin, P.; Zhikharev, V.; Okhapkin, A.; Ermakov, S. Epiplastic Algal Communities on Different Types of Polymers in Freshwater Bodies: A Short-Term Experiment in Karst Lakes. Water 2024, 16, 3288. https://doi.org/10.3390/w16223288

AMA Style

Vodeneeva E, Pichugina Y, Zhurova D, Sharagina E, Kulizin P, Zhikharev V, Okhapkin A, Ermakov S. Epiplastic Algal Communities on Different Types of Polymers in Freshwater Bodies: A Short-Term Experiment in Karst Lakes. Water. 2024; 16(22):3288. https://doi.org/10.3390/w16223288

Chicago/Turabian Style

Vodeneeva, Ekaterina, Yulia Pichugina, Darja Zhurova, Ekaterina Sharagina, Pavel Kulizin, Vyacheslav Zhikharev, Alexander Okhapkin, and Stanislav Ermakov. 2024. "Epiplastic Algal Communities on Different Types of Polymers in Freshwater Bodies: A Short-Term Experiment in Karst Lakes" Water 16, no. 22: 3288. https://doi.org/10.3390/w16223288

APA Style

Vodeneeva, E., Pichugina, Y., Zhurova, D., Sharagina, E., Kulizin, P., Zhikharev, V., Okhapkin, A., & Ermakov, S. (2024). Epiplastic Algal Communities on Different Types of Polymers in Freshwater Bodies: A Short-Term Experiment in Karst Lakes. Water, 16(22), 3288. https://doi.org/10.3390/w16223288

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