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The first evidence of microplastics in plant-formed fresh-water micro-ecosystems: Dipsacus teasel phytotelmata in Slovakia contaminated with MPs
expand article infoKatarína Fogašová, Peter Manko, Jozef Oboňa
‡ University of Prešov, Prešov, Slovakia
Open Access

Abstract

Tiny pieces of plastic, or microplastics, are one of the emerging pollutants in a wide range of different ecosystems. However, they have, thus far, not been confirmed from phytotelmata – specific small water-filled cavities provided by terrestrial plants. The authors confirmed microplastics (141 μm – 2.4 mm long fibres of several colour and blue and orange fragments with diameters of 9–81 μm) in quantities from 101 to 409 per ml in Dipsacus telmata from two different periods. The phytotelmata, therefore, appear to be possible indicators of current and future microplastic pollution of the environment. However, further research is needed to obtain accurate information and verify the methodology for possible assessment of the local environmental burden of microplastics.

Keywords

plants, plastics, transport, telmata

Introduction

Microplastics (MPs) are becoming an important problem (e.g. Andrady 2011; Cole et al. 2011; Weber et al. 2021 etc.). They have been recorded in a wide range of different ecosystems, from terrestrial to aquatic (e.g. de Souza Machado et al. 2018; Weber et al. 2021; Yang et al. 2021) and even in food, bottled drinking water and the organs of various organisms, including humans (e.g. Carbery et al. 2018; Jin et al. 2021; Ragusa et al. 2021). Most studies of MPs, or SAMPs (atmospheric MPs), are more focused on the marine and freshwater ecosystems (e.g. Panebianco et al. 2019; Weber et al. 2021; Yang et al. 2021) and we still do not have enough information about their impact on organisms (e.g. Al-Jaibachi et al. 2019).

To the authors’ knowledge, the presence of MPs has not yet been confirmed in phytotelmata, a wide range of generally non-permanent aquatic microecosystems in plants (e.g. Kitching 2000; Kanašová et al. 2020). Amongst the few phytotelmata in the temperate zone of Europe are dendrotelmata and phytotelmata provided by the teasel Dipsacus (e.g. Williams 1996, 2006; Kitching 2000; Oboňa et al. 2011; Oboňa and Svitok 2012; Kanašová 2017; Kanašová et al. 2020). Teasel phytotelmata (Fig. 1) are a relatively common, but overlooked aquatic microcosm with a very short-term occurrence of only 3 to 4 months (Kanašová et al. 2020). Dipsacus teasel has characteristic opposite leaves that grow on the stem above each other in several levels (the oldest near the soil surface and the youngest are the highest), clasping the stem and forming cup-like structures that collect water (water axil or telmata).

Figure 1.

Phytotelmata in the teasel Dipsacus.

The main purpose of the sampling was to describe the seasonal dynamics of organisms living in teasel telmata. The detection of MPs in these samples was accidental and unexpected. The objective of this paper is to describe the first documented evidence of MPs in phytotelmata.

Materials and methods

Water samples with sediment from phytotelmata on teasel Dipsacus came from two areas of eastern Slovakia (see Map. 1) near the villages of Demjata (49°6'58.578231"N, 21°18'47.3838982"E, Fig. 2) and Kapušany (49°3'12.6212568"N, 21°20'16.680325"E).

Map 1.

Location of the study areas.

Figure 2.

Locality of the teasels in Demjata.

The samples were obtained from five plants at each of two sampling localities at the end of each of five 14-day long collection periods from all levels of leaf axils at examined plants. The collection was carried out using standard methods (see Kanašová et al. 2020) using sterile containers. Therefore, contamination of the samples from another source is clearly excluded. These 50 sampled Dipsacus individuals provided 171 functioning phytotelmata. Altogether, 4596 ml of water and sediments were analysed (see Table 1).

Table 1.

Overview of sample volumes of individual phytotelmata.

Date Plant number Locality total levels on the plant level 1 level 2 level 3 level 4 level 5 level 6 level 7 level 8 level 9 level 10
sample number volume (ml) sample number volume (ml) sample number volume (ml) sample number volume (ml) sample number volume (ml) sample number volume (ml) sample number volume (ml) sample number volume (ml) sample number volume (ml) sample number volume (ml)
6/14/ 2021 1 Demjata 6 damaged damaged 1 38 2 29 3 17 empty
2 Demjata 6 1 12 2 14 3 21 empty empty empty
3 Demjata 6 damaged 1 70 2 37 3 13 empty empty
4 Demjata 7 damaged 1 37 2 85 3 17 empty empty empty
5 Demjata 7 1 15 2 8 3 16 4 35 5 10 empty empty
1 Kapušany 6 1 12.5 2 44 3 42 4 49 empty empty
2 Kapušany 7 1 17 2 16 3 26 4 6 empty empty empty
3 Kapušany 6 1 15 2 31 3 10 empty empty empty
4 Kapušany 6 damaged 1 4 2 16 3 7.5 4 3 empty
5 Kapušany 7 damaged damaged 1 35 2 4 empty empty empty
6/28/ 2021 1 Demjata 8 damaged damaged damaged 1 35 2 18 3 14 4 3 empty
2 Demjata 9 damaged 1 20 2 73 3 61 4 49 5 27 empty empty empty
3 Demjata 9 damaged damaged 1 6 2 76 3 61 4 47 5 11 empty empty
4 Demjata 9 damaged damaged 1 10 2 106 3 92 4 43 empty empty empty
5 Demjata 9 damaged 1 5 damaged 2 41 3 20 4 12 empty empty empty
1 Kapušany 8 damaged 1 5 2 51 3 41 4 60 5 45 6 20 7 15
2 Kapušany 9 damaged damaged damaged 1 42 2 37 3 26 4 25 5 5 empty
3 Kapušany 8 damaged damaged 1 29 2 42 3 80 4 34 5 29 6 6
4 Kapušany 8 damaged damaged 1 51 2 92 3 45 4 45 5 36 6 17
5 Kapušany 9 damaged damaged damaged 1 5 2 85 3 70 4 15 5 16 6 8
7/12/ 2021 1 Demjata 9 damaged damaged 1 50 2 36 3 20 4 10 empty damaged damaged
2 Demjata 9 damaged damaged 1 9 2 6 3 17 4 29 5 12 damaged damaged
3 Demjata 8 damaged damaged 1 7 2 10 3* 11* empty empty damaged
4 Demjata 8 damaged damaged 1 20 2 16 3 17 4 5 damaged damaged
5 Demjata 9 damaged damaged 1 20 2 60 3 25 4 14 5* 6* empty damaged
1 Kapušany 8 damaged 1* 9* 2 76 3 95 4 83 damaged 5 12 6 3
2 Kapušany 7 damaged 1 12 2 17 3 7 empty empty empty
3 Kapušany 7 damaged damaged damaged 1 7 2 5 empty empty
4 Kapušany 8 damaged damaged 1 32 2 47 3 24 damaged empty damaged
5 Kapušany 8 damaged 1 2 2 18 damaged 3 41 4 49 5 15 empty
7/26/ 2021 1 Demjata 7 damaged damaged 1* 8* empty empty damaged damaged
2 Demjata 8 damaged empty 1 9 2 2 empty empty empty damaged
3 Demjata 8 damaged damaged empty 1 10 empty empty empty damaged
4 Demjata 8 damaged damaged damaged 1 12 2 5 damaged damaged damaged
5 Demjata 8 damaged damaged 1 11 empty empty empty damaged damaged
1 Kapušany 8 damaged damaged 1 10 damaged 2* 40* empty 3 5 empty
2 Kapušany 9 damaged damaged 1 6 2 41 3 110 4 58 5 12 6 6 damaged
3 Kapušany 10 damaged damaged damaged damaged 1 15 2 12 empty empty damaged damaged
4 Kapušany 9 damaged damaged 1 5 2 55 3 55 4* 75* 5 11 empty damaged
5 Kapušany 8 damaged damaged damaged damaged 1 90 empty 2 9 empty
8/9/ 2021 1 Demjata 8 damaged damaged damaged 1 5 2 6 empty empty empty
2 Demjata 7 damaged damaged 1 8 2 5 3 3 empty empty
3 Demjata 8 damaged damaged damaged damaged 1 3 empty empty empty
4 Demjata 7 damaged damaged damaged 1 3 2 2 empty empty
5 Demjata 8 damaged damaged damaged damaged 1 5 empty empty empty
1 Kapušany 8 damaged damaged damaged damaged damaged damaged 1 15 empty
2 Kapušany 8 damaged damaged damaged 1 47 2 6 3 14 4 2 empty
3 Kapušany 8 damaged damaged damaged damaged 1 24 2 45 3 12 empty
4 Kapušany 7 damaged damaged damaged damaged 1 10 empty empty
5 Kapušany 7 damaged damaged damaged 1 36 empty empty empty

In the laboratory, the samples were examined using a microscope method after transfer to a sterile Petri dish. After first MP evidence, the examination was conducted following the microscopic method (see Yang et al. 2021). Positive samples were separated and MPs photographed and measured. From positive samples, we analysed 3 ml of the total sample volume. For the greatest possible accuracy, we analysed this volume in increments of 0.5 ml, always after thorough mixing of the liquid. Quantitative data were then converted to 1 ml of sample. These examinations and measurements were conducted using a Leica M205MC stereomicroscope (magnification of 7.8–160×), equipped with a Leica DFC295 digital camera. The minimal size of particles captured and measured by this method and equipment used is 1 µm.

Results and discussion

Overall, MPs were detected in only in 6 of 171 examined samples (incidence 3.5%). MPs consisted, in particular, of blue, black, red and white 141 μm to 2.4 mm long fibres and blue and orange fragments with diameters of 9 to 81 μm. There were 101 to 409 MPs in each positive sample (Table 2). Positive telmata were recorded only during two sampling periods (29.6.–12.7.2021 and 13.–26.7.2021) at different levels and always at both locations. These results are the first confirmation of evidence of MPs in phytotelmata on Dipsacus teasel (see Fig. 3).

Table 2.

The detailed information about MPs in positive phytotelmata.

Date Plant number Locality Total levels on the plant Level Sample number Volume (ml) Fibers Fragments Average amount of MPs per 1 ml
Total Number (3 ml) Colour Min. length (mm) Max. length (mm) Total Number (3 ml) Colour Min. size (mm) Max. size (mm) Fibres Fragments Total
Blue Black Red White Blue Orange
7/12/2021 3 Demjata 8 5 3 11 8 3 3 1 0 0.2051 1.5790 98 58 40 0.0107 0.0718 2.7 32.7 275.19
7/12/2021 5 Demjata 9 7 5 6 4 2 2 0 0 0.1558 1.3092 159 45 114 0.0096 0.0695 1.3 53.0 408.87
7/12/2021 1 Kapušany 8 2 1 9 12 6 3 0 3 0.1955 2.1730 22 15 7 0.0122 0.0420 4.0 7.3 101.75
7/26/2021 1 Demjata 7 3 1 8 3 3 0 0 0 0.1414 0.8832 142 28 114 0.0096 0.0528 1.0 47.3 358.42
7/26/2021 1 Kapušany 8 5 2 40 13 8 2 3 0 0.1663 2.3937 59 33 26 0.0115 0.0808 4.3 19.7 225.65
7/26/2021 4 Kapušany 9 6 4 75 0 0 0 0 0 0 0 56 18 38 0.0088 0.0551 0.0 18.7 224.73
Figure 3.

Microplastic fibre and fragments from a phytotelmata sample.

These phytotelmata are very small and have a short lifespan (e.g. Kanašová et al. 2020). The question is, therefore, how were they polluted with MPs? The most probable contamination source is suspended atmospheric SAMPs. Fibres (Liu et al. 2019; Wright et al. 2020) and fragments (Allen et al. 2019) are the most prevalent shapes in SAMPs samples and they also dominated in phytotelmata. Our findings also support the idea that SAMPs could have an MP pollution source (Alfonso et al. 2021), whereas other paths for the spread of fibres and fragments into above-ground phytotelmata are unlikely to be possible. In the case of SAMPs’ contamination, the low number of positive phytotelmata may be explained by the density of the surrounding vegetation and by the position and orientation of the water-filled cavities on Dipsacus.

The second possible pathway of contamination is zoonotic transport (active or passive) through snails (Fig. 4). Snails could transfer particles of MPs on or in their bodies (e.g. Panebianco et al. 2019). This theory can be supported by the frequent presence of living or drowned snails and their excrements in teasel phytotelma (see Fig. 5). Transmission by molluscs from soil and plant surfaces would indicate pollution from the earth’s surface. In any case, the surface of the landscape, soil and vegetation could only be contaminated by the atmosphere (SAMPs) at the sites examined in this study, as no other sources of contamination are present at the localities or in their immediate surroundings.

Figure 4.

The presence of snail (Cepaea) on teasel leaves.

Figure 5.

Microparticles in snail excrement.

Based on these results, aims in our future research will be: (1) to find out whether the pathway of pollution (i.e. wind transport, active zoonotic transport, passive zoonotic transport) would influence the utility of phytotelmata as indicators of microplastic pollution and (2) to test the hypothesis that the amount of microplastics in phytotelmata reflects their amount in the environment (i.e. more MPs in the environment mean more MPs in phytotelmata). Teasel phytotelmata are a relatively common, but overlooked aquatic microcosms (Kanašová et al. 2020). Due to their abundance and theoretical ability to capture MPs in several ways from the environment, they could be a good indicator of MPs occurrence (rather than directly measuring the environment). Moreover, the temporal character of phytotelmata and the succession of individual levels serves as a natural “time-lapse” sampling with the possibility of identifying temporal differences in the intensity of contamination during the growing season.

MPs have become one of the emerging pollutants in a wide range of different ecosystems (e.g. de Souza Machado et al. 2018; Carbery et al. 2018; Yang et al. 2021; Weber et al. 2021; Jin et al. 2021; Ragusa et al. 2021). The occurrence of MPs has continued to expand on a global scale and has attracted widespread attention from scientists, policy-makers and the public (e.g. Jin et al. 2021). One of the basic prerequisites for a solution and remediation is an understanding of the external forces that drive the transport and diffusion of these pollutants. Our findings point to the possibility of using phytotelmata (and/or artificial telmata) to determine the contamination of the environment by MPs and the relatively simple detection of seasonal/temporal changes in the atmospheric load of the studied sites by SAMPs. In any case, this topic and the bio-indicative potential of telmata in the environmental burden of MP assessment deserve further research and more attention.

Acknowledgements

We thank the editor and all anonymous reviewers for their valuable and constructive comments on the first versions of the manuscript. We also thank the kind and helpful Nathalie Yonow for the thorough proofreading of the second version of the manuscript, her important questions, comments and suggestions. This work was supported by the Slovak Scientific Grant Agency, contract No. VEGA-1/0012/20 and by the Grant Agency of University Prešov in Prešov under contract No. GaPU 6/2021.

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