- Email: [email protected]
Moss as a biomonitor for the atmospheric deposition of anthropogenic microfibres
Science of the Total Environment 715 (2020) 136973
Contents lists available at ScienceDirect
Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Short Communication
Moss as a biomonitor for the atmospheric deposition of anthropogenic microfibres Brett Roblin ⁎, Julian Aherne Trent University, Environmental and Life Science, Peterborough K9L 0G2, Canada
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
• Moss was evaluated as a biomonitor for the atmospheric deposition of anthropogenic microfibres. • Anthropogenic microfibres were observed in all moss samples, the average number was 24 g−1 dry weight. • Annual average atmospheric deposition of microfibres was estimated at ~47,700 m−2 across three remote catchments. • Trajectory analysis suggests that microfibres may be subject to longrange atmospheric transport.
a r t i c l e
i n f o
Article history: Received 20 December 2019 Received in revised form 26 January 2020 Accepted 26 January 2020 Available online 27 January 2020 Editor: Damia Barcelo Keywords: Microfibres Biomonitoring Moss Atmospheric deposition
a b s t r a c t Microplastics, which are plastic particles b 5 mm, have been found throughout the environment. However, few studies have focused on their transport via atmospheric deposition. Bryophytes have been used as biomonitors for the atmospheric deposition of trace elements, persistent organic pollutants and particulate matter, and may potentially be used to monitor the atmospheric deposition of microplastics or anthropogenic microfibres (mf). Hylocomium splendens was collected from three lake catchments, which are remote from anthropogenic disturbance and emissions sources. Anthropogenic mf were observed in all moss samples; the average number was 24 mf g−1 dry weight (range: 15–30 mf g−1) across the three study sites. The average length of mf was 1.02 mm (range: 0.83–1.20 mm). Plastic mf were identified using five rigorous visual criteria; 27% of the observed mf passed four criteria and 13% passed all five, suggesting at most a quarter of the mf may be plastic. Annual average atmospheric deposition of anthropogenic mf across the three lake catchments was estimated at ~47,700 mf m−2 (~12,000 plastic mf m−2), based on a moss biomass of 2 kg dry weight m−2. These preliminary findings suggest that moss may be a useful biomonitor for the atmospheric deposition of mf (and microplastics). © 2018 Published by Elsevier B.V.
1. Introduction Microplastics, which are plastic particles smaller than 5 mm, have gained increasing attention in the scientific literature during the last ⁎ Corresponding author. E-mail address: [email protected] (B. Roblin).
https://doi.org/10.1016/j.scitotenv.2020.136973 0048-9697/© 2018 Published by Elsevier B.V.
decade owing to their ubiquity in natural environments. These waste plastics are either manufactured to be microscopic in size or come from plastic bottles, bags, clothing, etc., that have broken down and fragmented through UV radiation, physical abrasion and biodegradation (Hidalgo-Ruz et al., 2012; Dris et al., 2015; Dris et al., 2016; Peng et al., 2017). One of the most common types of microplastics are microfibres (mf; Wesch et al., 2017), which come from textiles, nets, fishing line
2
B. Roblin, J. Aherne / Science of the Total Environment 715 (2020) 136973
and the fragmentation of larger plastic materials (Barrows et al., 2018; Cago et al., 2018). Microplastics (and mf) are considered an environmental contaminant due to their chemical additives (e.g., dyes) and risk of physical harm (blockage, abrasion) to organisms when ingested (Cole et al., 2011; Zhao et al., 2014; Wagner et al., 2014). In addition, persistent organic pollutants (POPs), and trace elements can be absorbed and potentially transported by microplastics (Hidalgo-Ruz et al., 2012; Zhang et al., 2016; Horton et al., 2017). Microplastics have been found in a variety of environments although the majority of studies have focused on marine systems (Wagner et al., 2014; Horton et al., 2017). More recently, several studies have focused on the atmospheric transport of microplastics, which are dominated by mf (Dris et al., 2016; Cai et al., 2017; Stanton et al., 2019; Allen et al., 2019; Wright et al., 2019), and their potential for long-range transport into terrestrial and aquatic environments (Horton et al., 2017; Horton and Dixon, 2018; Bergmann et al., 2019). However, these studies have predominantly focused on urban centres (Dris et al., 2016; Cai et al., 2017; Stanton et al., 2019; Wright et al., 2019); as such, the extent of transport via atmospheric deposition is not fully understood (Horton and Dixon, 2018). The collection of mf fallout in atmospheric deposition requires monitoring equipment, which is generally limited to a few fixed monitoring locations. Their assessment is time consuming and existing atmospheric networks can only provide limited information on the regional variation of atmospheric mf deposition. Biological monitors, or biomonitors, are living organisms that can be used for monitoring the abundance or determining the presence of an anthropogenic pollutant. Bryophytes, specifically mosses, have been widely used to assess the atmospheric deposition of trace elements (Berg et al., 1995; Halleraker et al., 1998; Schintu et al., 2005). Mosses typically form large mats that have high surface areas and absorb trace elements (gases and particles) from the atmosphere (Aceto et al., 2003; Schintu et al., 2005; Suchara et al., 2011). The use of moss as a biomonitor has been widely adopted since the late 1960s following studies that showed Hylocomium splendens was able to accumulate and retain metals from atmospheric deposition (Rühling and Tyler, 1968; Rühling and Tyler, 1970). Similarly, Pleurozium schreberi, Hypnum cupressiforme, and Pseudoscleropodium purum (and many other species) have been widely used as biomonitors for atmospheric deposition, with large scale surveys repeated across Europe every five years under the co-ordination of the International Cooperative Programme on Effects of Air Pollution on Natural Vegetation and Crops (ICP Vegetation) since 1990 (Harmens et al., 2010). Moss has been successfully used to monitor the atmospheric deposition of trace elements (Berg et al., 1995; Halleraker et al., 1998; Schintu et al., 2005; Harmens et al., 2010; Wilkins and Aherne, 2015; Cowden and Aherne, 2019), nitrogen (Harmens et al., 2011; Olmstead and Aherne, 2019), POPs (Harmens et al., 2013) and particulate matter (Clough, 1975; Adamo et al., 2008). The objective of this preliminary study was to assess the use of moss as a biomonitor for the atmospheric deposition of anthropogenic mf. The moss species Hylocomium splendens was collected from three lake catchments in Ireland during summer 2018, all catchments were remote from anthropogenic activity and industrial emissions sources. All samples were analysed for the presence of mf, which have been shown to be dominant in atmospheric deposition (Dris et al., 2016; Cai et al., 2017; Wright et al., 2019).
this study are part of the International Cooperative Programme for assessment and monitoring of the effects of air pollution on rivers and lakes (ICP Waters). The lakes have been sampled for water chemistry (major ions) since the mid-1980s (Bowman, 1986, 1991). All locations are remote from point source influences of anthropogenic activity and located in National Parks, or protected areas, far from urban centres (Table 1). Glendalough Upper is in the Wicklow Mountains National Park, Lough Maumwee is a private lake for recreational fishing managed by the Corrnamona Angling Club, and Lough Veagh is in the Glenveagh National Park (Fig. 1; Supporting information Fig. SI-1). The lake catchments have similar annual average air temperatures but vary in annual rainfall (Table 1). The primary wind direction to the lake catchments is from the West and West Southwest (see Supporting information Fig. SI2). 2.2. Field sampling The moss species Hylocomium splendens was collected from each lake catchment during 11–14 May 2018 following the widely used survey protocols recommended by ICP Vegetation (ICPV, 2015). At each study site, a composite sample of moss was collected from N5 locations by hand (wearing nitrile gloves) from a 50 m2 plot to provide a representative estimate of deposition; samples were collected away from tree canopy cover, trails, and roads or any anthropogenic activity. The samples (~5 g wet weight) were stored in 500 mL HDPE jars that were triple rinsed prior to sampling with filtered B-pure™ water (ideally 500 mL glass jars should be used to avoid potential contamination; in the current study HDPE jars were used owing to concerns of breakage during transport). 2.3. Microfibre extractions In the laboratory, moss samples were dried at 50°C for 48 h. Under a fume hood (laminar flow cabinet), triplicate 1 g moss samples for each site (and the remaining mass as a fourth sample per site) were digested using a wet peroxide oxidation method (Masura et al., 2015; Herrera et al., 2018). The digestion procedure was carried out by adding 40 mL of 0.05 M Fe (II) solution to each moss sample; 40 mL of 30% hydrogen peroxide (H2O2) was subsequently added and the mixture was left at room temperature for 5 min. The digestate was heated to between 40 and 50°C to increase the reaction, and a further 20 mL aliquot of H2O2 was added when the reaction slowed down, if organic matter was still visible; at least three aliquots were added to each sample. Samples were then vacuum filtered onto glass-fibre filter papers (Fisherbrand™ G6 [09-804-42A]: 1.6 μm, following Dris et al., 2016) and dyed with 1 mL of Rose Bengal (4,5,6,7-tetrachloro-2′,4′,5′,7′-tetraiodofluorescein, 200 mg L−1) to help visually distinguish synthetic material from organic matter following Liebezeit and Liebezeit (2014) and Kosuth et al. (2018), i.e., the non-stained material is typically assumed to be synthetic as Rose Bengal is a biological stain that should bind to natural fibres. In the current study, Rose Bengal was not used to conclusively identify plastic fibres, rather it was only used to aid in the identification procedure. Finally, the moss sampling jars were rinsed with (filtered) Bpure™ water and filtered to capture residual fibres. The dyed filter papers (four per study site) were transferred to petri dishes for storage and for assessment of mf.
2. Materials and methods 2.4. Microscopy and microfibre identification 2.1. Study sites Ireland is situated on the western periphery of Europe and predominantly receives clean air masses from the Atlantic Ocean. As such, observations on the West coast of Ireland have been used as a European reference for transboundary air pollution, e.g., the Mace Head Atmospheric Research Station has been used as a reference site for many pollutants (e.g., Derwent et al., 2007). The three lake catchments used in
The filter papers were analysed for the presence of mf using a stereomicroscope (Leica EZ4W with EZ4W0170 camera) following a five criteria visual identification method modified from Norén (2007) and Windsor et al. (2018). It has been shown that identification of mf according to standardized criteria in connection with strict and conservative examination reduces the possibility of misidentification (Norén, 2007). Further, Löder and Gerdts (2015) demonstrated that for
B. Roblin, J. Aherne / Science of the Total Environment 715 (2020) 136973
3
Table 1 Site description, including coordinates, elevation (EL), long-term average annual air temperature (AT) and annual rainfall (AP) taken from the nearest meteorological station (URL: www. met.ie), and lake surface water concentrations for non-marine sulphate and nitrate during summer 2018 (markers of anthropogenic air pollutant emissions) for the three study catchments. Lake catchment
Latitude
Longitude
Decimal degrees Glendalough Lough Maumwee Lough Veagh
53.00281 53.47672 55.03822
−6.36806 −9.54092 −7.97269
EL
AT
AP
Sulphate −1
m ASL
°C
mm year
μeq L
133 50 43
9.7 10.5 9.9
754 1228 1093
62.7 52.2 55.7
particles N 0.5 mm, visual analyses are suitable for identification. The five criteria were: (i) the fibre is unnaturally coloured (blue, red, green, purple, black, grey) compared with other particles/detritus; (ii) the fibre appears homogenous in material and texture with no visible cell structure or offshoots and is a consistent width throughout its entire length; (iii) the fibre remains intact and is not brittle when compressed, tugged or poked with fine tweezers; (iv) the fibre has a shiny or glossy appearance; and (v) there is limited fraying with no similarities to natural fibres (see Supporting information Table SI-1). It is recommended that at least two of the criteria be met for a fibre to be classified as a microplastic (Windsor et al., 2018). Previous studies have classified all fibres not stained by Rose Bengal as ‘microplastic’ (Liebezeit and Liebezeit, 2014), while others have chosen to use the more general term ‘anthropogenic debris’ (Kosuth et al., 2018). In the current study, non-stained fibres that met two of the criteria were classified as anthropogenic mf; however, the proportion of fibres that met three, four and five criteria were also recorded, with the assumption that fibres that met four–five criteria were more likely plastic. Each mf (that meet two criteria) was photographed and its length was measured using ImageJ processing software (see Supporting information Table SI-2 and Fig. SI-3). It is recognised that only spectroscopic analysis (Fourier Transform infrared (FT-IR) or Raman spectroscopy) can provide unambiguous proof of the synthetic nature of the
−1
Nitrate μeq L−1 15.9 5.6 7.4
non-stained fibres. A small number of fibres were analysed by Raman spectroscopy in the current study (see Supporting information Fig. SI4). 2.5. Quality control and data analysis Throughout sample processing and analysis, procedural open-air blanks were used to determine the amount of potential contamination; open-air and digestion (process) blanks were used during filtering, digesting and oven drying. Digestion blanks were completed by using filtered B-pure™ in place of the sample media during the digestion process. Triplicate B-pure™ water blanks (1 L) were initially vacuum filtered and analysed following the same method as the moss samples to determine the level of mf contamination; the average number of mf in B-pure™ blanks was 11.4 mf L−1 (coefficient of variation of 112%). As such, all B-pure™ water was filtered (Fisherbrand G6: 1.6 μm) prior to use for cleaning and extraction (use in FE(II) solution and Rose Bengal) to avoid potential contamination. Further, during mf extraction (digesting and filtering), samples were covered with aluminium foil to prevent airborne contamination (following Dris et al., 2016; Koelmans et al., 2019; Wright et al., 2019), and all equipment was rinsed with filtered B-pure™ water prior to use. Peroxide blanks (1 L in total) were also vacuum filtered and analysed following the same method as the moss samples to determine the level of mf contamination. Finally, 100% cotton clothes were worn during sample collection, and 100% cotton laboratory coats were worn when extracting and analysing the samples. Where possible the analysis adhered to quality criteria as identified by Koelmans et al. (2019). The number of mf per g (mf g−1) dry moss was calculated using the total mass of moss for each site (which included the fourth digestion and residual fibres in the sampling jar). The coefficient of variation (or relative standard deviation) was used to assess the spread in triplicate 1 g samples. The number of mf per g of dry moss were scaled to atmospheric deposition using published values for the biomass of moss, i.e., 2 kg dry weight m−2 (Forman, 1969; Singh et al., 2005). The longterm atmospheric source regions for each site was evaluated using source-receptor trajectory rose plots (arrival height of 850 hPa) based on two-day back trajectories estimated every 6 h during the period 1989–2009 (see Supporting information Fig. SI-2). Further, the water − concentrations of non-marine sulphate (SO2− 4 ) and nitrate (NO3 ) in each lake during summer 2018 (Table 1) were used to determine the anthropogenic atmospheric influence on the catchments, due to their use as markers for anthropogenic air pollution emissions. 3. Results
Fig. 1. Location of moss (Hylocomium splendens) sampling sites at three lake catchments monitored under ICP Waters: Glendalough, Lough Maumwee and Lough Veagh.
In total there were 28 filter blanks used to estimate the potential contamination of mf from open-air, water, H2O2 and digestion exposure. The average contamination was approximately 0.6 mf g−1 across all sites, i.e., b2.5 mf per site. Only five fibres were observed across all the open-air blanks (n = 20); the largest source of contamination was the unfiltered H2O2, which had 5 mf L−1 (variation between replicates of 40%). The contamination observed for the digestion blanks (n = 3) was 0.33 mf per sample. Given the overall low number, observations were not corrected for contamination in the current study.
4
B. Roblin, J. Aherne / Science of the Total Environment 715 (2020) 136973
Anthropogenic mf were observed in all moss samples (e.g., Supporting information Fig. SI-3) across the three study sites (Table 1); in total 300 mf were recorded across the three sites, ranging from 56 at Lough Maumwee to 162 at Glendalough (Table 2). The average number per site was 24 mf g−1 dry moss (Table 2). The ranged in triplicate moss (1 g) samples was 13–34 mf g−1 at Glendalough, 6–19 mf g−1 at Lough Maumwee, and 8–33 mf g−1 at Lough Veagh (see Supporting information Table SI-2). Glendalough had the least variation between triplicate samples with a coefficient of variation of 46% (Table 2) compared with Lough Maumwee (60%) and Lough Veagh (85%). Given the wide variation in triplicates, larger moss samples potentially provide a more accurate estimate of mf deposition. The length of anthropogenic mf ranged from 0.03–30.25 mm (Fig. 2; see Supporting information Table SI-2) with the longest at each of the sites at 30.25 mm (Glendalough), 3.94 mm (Lough Maumwee) and 4.31 mm (Lough Veagh). The average size of mf was 1.02 mm across the three sites (Table 2), ranging from 0.76 mm (Lough Maumwee) to 1.20 mm (Glendalough). Microfibres observed on moss were predominately b0.8 mm (65%), whereas mf N2 mm only made up 10% (Fig. 2). The coefficient of variation in mf length for the triplicate (1 g) samples ranged from 31% (Lough Veagh) to 42% (Lough Maumwee). To some extent, the most remote site (Lough Maumwee) has the lowest number of fibres and the smallest length of fibre (Table 2). The atmospheric deposition of mf across the three sites was estimated to be ~47,700 mf m−2 (Table 2). Glendalough had the highest estimated deposition at 58,900 mf m−2 followed by Lough Veagh (48,000 mf m−2) and Lough Maumwee (30,600 mf m−2). The proportion of anthropogenic mf that met three or more of the visual assessment criteria, was 70% (three criteria), 27% (four), and 13% met all five criteria (Table 3), suggesting that 13–27% of anthropogenic mf were plastic. Accordingly, the average deposition of plastic mf was estimated to be 6200–12,900 mf m−2. The indicators of anthropogenic atmospheric pollutant deposition (Table 1), non-marine sulphate and nitrate, showed a similar pattern (site ranking) to the anthropogenic mf results (i.e., lowest to highest) Lough Maumwee, Lough Veagh and Glendalough (Table 2); Glendalough had higher concentrations of sulphate and nitrate (62.7 μeq L−1 and 15.9 μeq L−1) compared with Lough Maumwee −1 −1 (52.2 μeq SO2− and 5.6 μeq NO− ). Similarly, the dominant air 4 L 3 L source region to the lakes (i.e., Republic of Ireland and Great Britain), showed a similar pattern to the mf results, i.e., Glendalough had the highest proportion of air from anthropogenic source regions. The correspondence between the number of mf, level of anthropogenic pollutants and air source region, suggests that mf may be subject to longrange atmospheric transport. 4. Discussion Microfibres were observed in all moss samples collected from three lake catchments located in rural regions. The ability of moss to entrap and retain microscopic particles implies that it is a reliable biomonitor of atmospheric mf deposition. Nonetheless, few studies have evaluated moss as a biomonitor for mf; one recent study evaluated the Table 2 The number of microfibres (mf), number per mass (coefficient of variation between triplicates), estimated deposition and average length of mf (coefficient of variation between triplicate 1 g samples) at the three study sites (total mass of moss digested is also shown). Site (mass of moss)
Glendalough (5.50 g) Lough Maumwee (3.66 g) Lough Veagh (3.41 g) Total/average (12.57 g) a
effectiveness of the aquatic moss Sphagnum palustre L. as a biomonitor of microplastics in freshwater environments (Capozzi et al., 2018). Contamination is a concern when dealing with mf. The average contamination was approximately 0.6 mf g−1 across all sites, i.e., b2.5 mf per site. Only five fibres were observed across all the open-air blanks (n = 20); the largest source of contamination was the unfiltered H2O2, which had 5 mf L−1 (variation between replicates of 40%). Given the overall low number, the observation mf in moss samples were assumed to reflect atmospheric deposition. Average atmospheric deposition of mf was estimated to be ~47,700 mf m−2 across the three lake catchments, based on published estimates for the biomass of moss (Table 2). However, moss biomass can vary greatly by site and species of moss; as such, further measurements are needed to accurately scale-up observations on moss to regional deposition. The living green portion of Hylocomium splendens (collected in this study) is considered to represent the last 2–3 years of growth; as such, the estimated deposition may represent a cumulative 2–3 years of deposition. Nonetheless, estimated mf deposition in the current study was similar in magnitude to previous studies that evaluated deposition, e.g., annual atmospheric deposition of mf in in Paris (~30,000 mf m−2 [n = 2]), France, Dongguan city (~72,000 mf m−2 [n = 3]; estimated from three months), China, Nottingham (~27,000 mf m−2 [n = 4]), England, and the Pyrenees mountains (~16,000 mf m−2 [n = 1]; estimated from five months), France (Dris et al., 2016; Cai et al., 2017; Stanton et al., 2019; Allen et al., 2019). The average length of mf observed in this study was 1.02 mm, with ~40% shorter than 0.4 mm (Fig. 2); in contrast, in urban Paris and Dongguan ~40–45% of the observed mf were shorter than 0.6–0.7 mm (Dris et al., 2016; Cai et al., 2017). In the current study, there was a higher proportion of shorter mf at sites more remote from urban centres, e.g., Glendalough, which is on east coast of Ireland and closest to a large population centre (b50 km from Dublin), had the longest fibres (1.20 mm). In contrast, Lough Maumwee, which is more strongly influenced by Atlantic air currents, had the shortest fibres (0.76 mm), suggesting that smaller fibres are more likely to be transported in the atmosphere and make up a higher proportion of the total number of fibres at more remote sites. Further, the number of anthropogenic mf per site was consistent with the level of anthropogenic pollutants and source-receptor analysis, i.e., the study sites had an anthropogenic atmospheric influence in the order of Glendalough N Lough Veagh N Lough Maumwee, which was consistent with the total number and average length of mf observed at the sites (Tables 1 and 2). On average, only 13% of the observed mf passed all five identification criteria and 27% passed four criteria per site (Table 3). In the current study, it was assumed that mf that met four or five identification criteria, had a greater likelihood of being plastics, i.e., 13–27% of mf were microplastics. This range was similar to previous studies, e.g., the proportion of plastic mf in atmospheric deposition was estimated to be 23% in Dongguan City, China, and 29% in urban Paris, France, based on FT-IR spectroscopy (Dris et al., 2016; Cai et al., 2017). It is difficult to unambiguously visually-discriminate all potential microplastic particles; error rates of visual sorting are reported to range from 20% (Eriksen et al., 2013) to 70% (Hidalgo-Ruz et al., 2012) and increase with decreasing particle size. Further, with respect to mf, Stanton et al. (2019) suggest that airborne fibre populations are largely dominated (N90%) by ‘natural’ textile, rather than microplastic fibres, which is consistent with the current study (13–27%).
Microfibres
Microfibres
Depositiona
Average length
5. Conclusions
n
n g−1
mf m−2
mm
162 56 82 300
29.5 (46%) 15.3 (60%) 24.0 (85%) 23.9
58,900 30,600 48,000 47,700
1.20 (36%) 0.76 (42%) 0.83 (31%) 1.02
Anthropogenic mf were observed in moss samples collected from remote lake catchments in Ireland; the magnitude and length of mf were similar to previous atmospheric studies. These preliminary results suggest that bryophytes may be a suitable biomonitor for the atmospheric deposition of mf. Furthermore, the relative magnitude of air from anthropogenically impacted regions, as indicated by trajectory analysis
Based on a biomass of 2 kg dry weight m−2.
B. Roblin, J. Aherne / Science of the Total Environment 715 (2020) 136973
5
Fig. 2. Size distribution (μm) of anthropogenic microfibres (n = 300) extracted from moss samples collected at three ICP Waters lake catchments (see Fig. 1).
and lake chemistry analysis, was consistent with the number of anthropogenic mf observed at each site, suggesting that mf may be subject to long-range atmospheric transport.
Author contributions BR conducted the field sampling, microfibre extractions, microscopy and microfibre identification. BR and JA designed the study, carried out the data analysis, wrote the main manuscript and prepared the figures.
Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements We gratefully acknowledge the Irish Environmental Protection Agency for funding this study (2016-CCRP-MS.43) and thank the National Parks and Wildlife Service, Inland Fisheries and the Corrnamona Angling Club for site access and logistical support. Finally, we would like to thank Hazel Cathcart for field assistance. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.scitotenv.2020.136973. Table 3 The percent of anthropogenic fibres that met three, four and five of the visual identification criteria per site (Glendalough, Lough Maumwee and Lough Veagh). The average across the three sites along with the average length is also given. Site
3 of 5 criteria
4 of 5 criteria
5 of 5 criteria
Glendalough Lough Maumwee Lough Veagh Average Length (mm)
69% 71% 71% 70% 1.00
27% 23% 28% 27% 1.01
15% 14% 10% 13% 1.92
References Aceto, M., et al., 2003. The use of mosses as environmental metal pollution indicators. Chemosphere 50, 333–342. Adamo, P., Giordano, S., Naimo, D., Bargagli, R., 2008. Geochemical properties of airborne particulate matter (PM10) collected by automatic device and biomonitors in a Mediterranean urban environment. Atmos. Environ. 42, 346–357. Allen, S., et al., 2019. Atmospheric transport and deposition of microplastics in a remote mountain catchment. Nat. Geosci. 12, 339–344. Barrows, A.P., Cathey, S., Peterson, C., 2018. Marine environment microfiber contamination: global patterns and the diversity of microparticle origins. Environ. Pollut. 237, 275–284. Berg, T., Røyset, O., Steinnes, E., 1995. Moss (Hylocomium splendens) used as biomonitor of atmospheric trace element deposition: estimation of uptake efficiencies. Atmos. Environ. 29, 353–360. Bergmann, M., Mützel, S., Primpke, S., Tekman, M., Trachsel, J., Gerdts, G., 2019. White and wonderful? Microplastics prevail in snow from the Alps to the Arctic. Sci. Adv. 5 (8), EAAX1157. Bowman, J., 1986. Precipitation Characteristics and the Chemistry and Biology of Poorly Buffered Irish Lakes: A Western European Baseline for ‘Acid Rain’ Impact Assessment. An Foras Forbartha, Dublin WR/G14. Bowman, J., 1991. Acid Sensitive Surface Waters in Ireland. Environmental Research Unit, Dublin, Ireland, p. 321. Cago, J., Carretero, O., Filgueiras, A., Vinas, L., 2018. Synthetic microfibers in the marine environment: a review on their occurrence in seawater and sediments. Mar. Pollut. Bull. 127, 365–376. Cai, L., et al., 2017. Characteristic of microplastics in the atmospheric fallout from Dongguan city, China: preliminary research and first evidence. Environ. Sci. Pollut. Res. 24, 24928–24935. Capozzi, F., Carotenuto, R., Giordano, S., Spagnuolo, V., 2018. Evidence on the effectiveness of mosses for biomonitoring of microplastics in fresh water environment. Chemosphere 205, 1–7. Clough, W., 1975. The deposition of particles on moss and grass surfaces. Atmos. Environ. 9, 1113–1119. Cole, M., Lindeque, P., Halsband, C., Galloway, T.S., 2011. Microplastics as contaminants in the marine environment: a review. Mar. Pollut. Bull. 62, 2588–2597. Cowden, P., Aherne, J., 2019. Assessment of atmospheric metal deposition by moss biomonitoring in a region under the influence of a long standing active aluminium smelter. Atmos. Environ. 201, 84–91. Derwent, R., Simmonds, P., Manning, A., Spain, T., 2007. Trends over a 20-year period from 1987 to 2007 in surface ozone at the atmospheric research station, Mace Head, Ireland. Atmos. Environ. 41, 9091–9098. Dris, R., et al., 2015. Microplastic contamination in an urban area: a case study in Greater Paris. Environ. Chem. 12 (2015), 592–599. Dris, R., Gasperi, J., Saad, M., Mirande, C., Tassin, B., 2016. Synthetic fibers in atmospheric fallout: a source of microplastics in the environment? Mar. Pollut. Bull. 104, 290–293. Eriksen, M., et al., 2013. Microplastic pollution in the surface waters of the Laurentian Great Lakes. Mar. Pollut. Bull. 77, 177–182. Forman, R., 1969. Comparison of coverage, biomass, and energy as measures of standing crop of bryophytes in various ecosystems. Bull. Torrey. Bot. Club 96, 582. Halleraker, J., et al., 1998. Reliability of moss (Hylocomium splendens and Pleurozium schreberi) as a bioindicator of atmospheric chemistry in the Barents region: interspecies and field duplicate variability. Sci. Total Environ. 218, 123–139.
6
B. Roblin, J. Aherne / Science of the Total Environment 715 (2020) 136973
Harmens, H., et al., 2010. Mosses as biomonitors of atmospheric heavy metal deposition: spatial patterns and temporal trends in Europe. Environ. Pollut. 158, 3144–3156. Harmens, H., et al., 2011. Nitrogen concentrations in mosses indicate the spatial distribution of atmospheric nitrogen deposition in Europe. Environ. Pollut. 159, 2852–2860. Harmens, H., Foan, L., Simon, V., Mills, G., 2013. Terrestrial mosses as biomonitors of atmospheric POPs pollution: a review. Environ. Pollut. 173, 245–254. Herrera, A., et al., 2018. Novel methodology to isolate microplastics from vegetal-rich samples. Mar. Pollut. Bull. 129 (1), 61–69. Hidalgo-Ruz, V., Gutow, L., Thompson, R.C., Thiel, M., 2012. Microplastics in the marine environment: a review of the methods used for identification and quantification. Environ. Sci. Technol. 46, 3060–3075. Horton, A., Dixon, S., 2018. Microplastics: an introduction to environmental transport processes. Wiley Interdiscip. Rev. Water 5, e1268. Horton, A.A., Walton, A., Spurgeon, D.J., Lahive, E., Svendsen, C., 2017. Microplastics in freshwater and terrestrial environments: evaluating the current understanding to identify the knowledge gaps and future research priorities. Sci. Total Environ. 586, 127–141. International Cooperation Programme Vegetation (ICPV), 2015. Monitoring of Atmospheric Deposition of Heavy Metals, Nitrogen and POPs in Europe Using Bryophytes. Monitoring Manual. Koelmans, A.A., Nor, N.H.M., Hermsen, E., Kooi, M., Mintenig, S.M., De France, J., 2019. Microplastics in freshwaters and drinking water: critical review and assessment of data quality. Water Res. 155, 410–422. Kosuth, M., Mason, S.A., Wattenberg, E.V., 2018. Anthropogenic contamination of tap water, beer, and sea salt. PLoS One 13, e0194970. Liebezeit, G., Liebezeit, E., 2014. Synthetic particles as contaminants in German beers. Food Addit. Contam. Part A 31, 1574–1578. Löder, M.G.J., Gerdts, G., 2015. In: Bergmann, M., Gutow, L., Klages, M. (Eds.), Marine Anthropogenic Litter. Springer, Cham, pp. 201–227. Masura, J., Baker, J., Foster, G., Arthur, C., 2015. Laboratory methods for the analysis of microplastics in the marine environment: recommendations for quantifying synthetic particles in waters and sediments. NOAA Technical Memorandum NOSOR&R-48. Norén, F., 2007. Small Plastic Particles in Coastal Swedish Waters. KIMO, Sweden. Olmstead, E., Aherne, J., 2019. Are tissue concentrations of Hylocomium splendens a good predictor of nitrogen deposition? Atmos. Pollut. Res. 10, 80–87.
Peng, J., Wang, J., Cai, L., 2017. Current understanding of microplastics in the environment: occurrence, fate, risks, and what we should do. Integr. Environ. Assess. Manag. 13, 476–482. Rühling, A., Tyler, G., 1968. An ecological approach to the lead problem. Bot. Notiser 121, 321–342. Rühling, Å., Tyler, G., 1970. Sorption and retention of heavy metals in the woodland moss Hylocomium splendens (Hedw.) Br. et Sch. Oikos 21, 92. Schintu, M., Cogoni, A., Durante, L., Cantaluppi, C., Contu, A., 2005. Moss (Bryum radiculosum) as a bioindicator of trace metal deposition around an industrialised area in Sardinia (Italy). Chemosphere 60, 610–618. Singh, M., et al., 2005. Preliminary estimation of bryophyte biomass and carbon pool from three contrasting different vegetation types. Cereal Research Communications 33, 267–270. Stanton, T., Johnson, M., Nathanail, P., MacNaughtan, W., Gomes, R., 2019. Freshwater and airborne textile fibre populations are dominated by ‘natural’, not microplastic, fibres. Sci. Total Environ. 666, 377–389. Suchara, I., et al., 2011. The performance of moss, grass, and 1- and 2-year old spruce needles as bioindicators of contamination: a comparative study at the scale of the Czech Republic. Sci. Total Environ. 409, 2281–2297. Wagner, M., et al., 2014. Microplastics in freshwater ecosystems: what we know and what we need to know. Environ. Sci. Eur. 26, 1–9. Wesch, C., et al., 2017. Assuring quality in microplastic monitoring: about the value of clean-air devices as essentials for verified data. Sci. Rep. 7. Wilkins, K., Aherne, J., 2015. Isothecium myosuroides and Thuidium tamariscinum mosses as bioindicators of nitrogen and heavy metal deposition in Atlantic oak woodlands. Ann. Bot. (Roma) 5, 71–78. Windsor, F., Tilley, R., Tyler, C., Ormerod, S., 2018. Microplastic ingestion by riverine macroinvertebrates. Sci. Total Environ. 646, 68–74. Wright, S.L., Ulke, J., Font, A., Chan, K.L.A., Kelly, F.J., 2019. Atmospheric microplastic deposition in an urban environment and an evaluation of transport. Environ. Int. 105411. Zhang, K., et al., 2016. Microplastic pollution of lakeshore sediments from remote lakes in Tibet plateau, China. Environ. Pollut. 219, 450–455. Zhao, S., Zhu, L., Wang, T., Li, D., 2014. Suspended microplastics in the surface water of the Yangtze Estuary System, China: first observations on occurrence, distribution. Mar. Pollut. Bull. 86, 562–568.
Contents lists available at ScienceDirect
Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Short Communication
Moss as a biomonitor for the atmospheric deposition of anthropogenic microfibres Brett Roblin ⁎, Julian Aherne Trent University, Environmental and Life Science, Peterborough K9L 0G2, Canada
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
• Moss was evaluated as a biomonitor for the atmospheric deposition of anthropogenic microfibres. • Anthropogenic microfibres were observed in all moss samples, the average number was 24 g−1 dry weight. • Annual average atmospheric deposition of microfibres was estimated at ~47,700 m−2 across three remote catchments. • Trajectory analysis suggests that microfibres may be subject to longrange atmospheric transport.
a r t i c l e
i n f o
Article history: Received 20 December 2019 Received in revised form 26 January 2020 Accepted 26 January 2020 Available online 27 January 2020 Editor: Damia Barcelo Keywords: Microfibres Biomonitoring Moss Atmospheric deposition
a b s t r a c t Microplastics, which are plastic particles b 5 mm, have been found throughout the environment. However, few studies have focused on their transport via atmospheric deposition. Bryophytes have been used as biomonitors for the atmospheric deposition of trace elements, persistent organic pollutants and particulate matter, and may potentially be used to monitor the atmospheric deposition of microplastics or anthropogenic microfibres (mf). Hylocomium splendens was collected from three lake catchments, which are remote from anthropogenic disturbance and emissions sources. Anthropogenic mf were observed in all moss samples; the average number was 24 mf g−1 dry weight (range: 15–30 mf g−1) across the three study sites. The average length of mf was 1.02 mm (range: 0.83–1.20 mm). Plastic mf were identified using five rigorous visual criteria; 27% of the observed mf passed four criteria and 13% passed all five, suggesting at most a quarter of the mf may be plastic. Annual average atmospheric deposition of anthropogenic mf across the three lake catchments was estimated at ~47,700 mf m−2 (~12,000 plastic mf m−2), based on a moss biomass of 2 kg dry weight m−2. These preliminary findings suggest that moss may be a useful biomonitor for the atmospheric deposition of mf (and microplastics). © 2018 Published by Elsevier B.V.
1. Introduction Microplastics, which are plastic particles smaller than 5 mm, have gained increasing attention in the scientific literature during the last ⁎ Corresponding author. E-mail address: [email protected] (B. Roblin).
https://doi.org/10.1016/j.scitotenv.2020.136973 0048-9697/© 2018 Published by Elsevier B.V.
decade owing to their ubiquity in natural environments. These waste plastics are either manufactured to be microscopic in size or come from plastic bottles, bags, clothing, etc., that have broken down and fragmented through UV radiation, physical abrasion and biodegradation (Hidalgo-Ruz et al., 2012; Dris et al., 2015; Dris et al., 2016; Peng et al., 2017). One of the most common types of microplastics are microfibres (mf; Wesch et al., 2017), which come from textiles, nets, fishing line
2
B. Roblin, J. Aherne / Science of the Total Environment 715 (2020) 136973
and the fragmentation of larger plastic materials (Barrows et al., 2018; Cago et al., 2018). Microplastics (and mf) are considered an environmental contaminant due to their chemical additives (e.g., dyes) and risk of physical harm (blockage, abrasion) to organisms when ingested (Cole et al., 2011; Zhao et al., 2014; Wagner et al., 2014). In addition, persistent organic pollutants (POPs), and trace elements can be absorbed and potentially transported by microplastics (Hidalgo-Ruz et al., 2012; Zhang et al., 2016; Horton et al., 2017). Microplastics have been found in a variety of environments although the majority of studies have focused on marine systems (Wagner et al., 2014; Horton et al., 2017). More recently, several studies have focused on the atmospheric transport of microplastics, which are dominated by mf (Dris et al., 2016; Cai et al., 2017; Stanton et al., 2019; Allen et al., 2019; Wright et al., 2019), and their potential for long-range transport into terrestrial and aquatic environments (Horton et al., 2017; Horton and Dixon, 2018; Bergmann et al., 2019). However, these studies have predominantly focused on urban centres (Dris et al., 2016; Cai et al., 2017; Stanton et al., 2019; Wright et al., 2019); as such, the extent of transport via atmospheric deposition is not fully understood (Horton and Dixon, 2018). The collection of mf fallout in atmospheric deposition requires monitoring equipment, which is generally limited to a few fixed monitoring locations. Their assessment is time consuming and existing atmospheric networks can only provide limited information on the regional variation of atmospheric mf deposition. Biological monitors, or biomonitors, are living organisms that can be used for monitoring the abundance or determining the presence of an anthropogenic pollutant. Bryophytes, specifically mosses, have been widely used to assess the atmospheric deposition of trace elements (Berg et al., 1995; Halleraker et al., 1998; Schintu et al., 2005). Mosses typically form large mats that have high surface areas and absorb trace elements (gases and particles) from the atmosphere (Aceto et al., 2003; Schintu et al., 2005; Suchara et al., 2011). The use of moss as a biomonitor has been widely adopted since the late 1960s following studies that showed Hylocomium splendens was able to accumulate and retain metals from atmospheric deposition (Rühling and Tyler, 1968; Rühling and Tyler, 1970). Similarly, Pleurozium schreberi, Hypnum cupressiforme, and Pseudoscleropodium purum (and many other species) have been widely used as biomonitors for atmospheric deposition, with large scale surveys repeated across Europe every five years under the co-ordination of the International Cooperative Programme on Effects of Air Pollution on Natural Vegetation and Crops (ICP Vegetation) since 1990 (Harmens et al., 2010). Moss has been successfully used to monitor the atmospheric deposition of trace elements (Berg et al., 1995; Halleraker et al., 1998; Schintu et al., 2005; Harmens et al., 2010; Wilkins and Aherne, 2015; Cowden and Aherne, 2019), nitrogen (Harmens et al., 2011; Olmstead and Aherne, 2019), POPs (Harmens et al., 2013) and particulate matter (Clough, 1975; Adamo et al., 2008). The objective of this preliminary study was to assess the use of moss as a biomonitor for the atmospheric deposition of anthropogenic mf. The moss species Hylocomium splendens was collected from three lake catchments in Ireland during summer 2018, all catchments were remote from anthropogenic activity and industrial emissions sources. All samples were analysed for the presence of mf, which have been shown to be dominant in atmospheric deposition (Dris et al., 2016; Cai et al., 2017; Wright et al., 2019).
this study are part of the International Cooperative Programme for assessment and monitoring of the effects of air pollution on rivers and lakes (ICP Waters). The lakes have been sampled for water chemistry (major ions) since the mid-1980s (Bowman, 1986, 1991). All locations are remote from point source influences of anthropogenic activity and located in National Parks, or protected areas, far from urban centres (Table 1). Glendalough Upper is in the Wicklow Mountains National Park, Lough Maumwee is a private lake for recreational fishing managed by the Corrnamona Angling Club, and Lough Veagh is in the Glenveagh National Park (Fig. 1; Supporting information Fig. SI-1). The lake catchments have similar annual average air temperatures but vary in annual rainfall (Table 1). The primary wind direction to the lake catchments is from the West and West Southwest (see Supporting information Fig. SI2). 2.2. Field sampling The moss species Hylocomium splendens was collected from each lake catchment during 11–14 May 2018 following the widely used survey protocols recommended by ICP Vegetation (ICPV, 2015). At each study site, a composite sample of moss was collected from N5 locations by hand (wearing nitrile gloves) from a 50 m2 plot to provide a representative estimate of deposition; samples were collected away from tree canopy cover, trails, and roads or any anthropogenic activity. The samples (~5 g wet weight) were stored in 500 mL HDPE jars that were triple rinsed prior to sampling with filtered B-pure™ water (ideally 500 mL glass jars should be used to avoid potential contamination; in the current study HDPE jars were used owing to concerns of breakage during transport). 2.3. Microfibre extractions In the laboratory, moss samples were dried at 50°C for 48 h. Under a fume hood (laminar flow cabinet), triplicate 1 g moss samples for each site (and the remaining mass as a fourth sample per site) were digested using a wet peroxide oxidation method (Masura et al., 2015; Herrera et al., 2018). The digestion procedure was carried out by adding 40 mL of 0.05 M Fe (II) solution to each moss sample; 40 mL of 30% hydrogen peroxide (H2O2) was subsequently added and the mixture was left at room temperature for 5 min. The digestate was heated to between 40 and 50°C to increase the reaction, and a further 20 mL aliquot of H2O2 was added when the reaction slowed down, if organic matter was still visible; at least three aliquots were added to each sample. Samples were then vacuum filtered onto glass-fibre filter papers (Fisherbrand™ G6 [09-804-42A]: 1.6 μm, following Dris et al., 2016) and dyed with 1 mL of Rose Bengal (4,5,6,7-tetrachloro-2′,4′,5′,7′-tetraiodofluorescein, 200 mg L−1) to help visually distinguish synthetic material from organic matter following Liebezeit and Liebezeit (2014) and Kosuth et al. (2018), i.e., the non-stained material is typically assumed to be synthetic as Rose Bengal is a biological stain that should bind to natural fibres. In the current study, Rose Bengal was not used to conclusively identify plastic fibres, rather it was only used to aid in the identification procedure. Finally, the moss sampling jars were rinsed with (filtered) Bpure™ water and filtered to capture residual fibres. The dyed filter papers (four per study site) were transferred to petri dishes for storage and for assessment of mf.
2. Materials and methods 2.4. Microscopy and microfibre identification 2.1. Study sites Ireland is situated on the western periphery of Europe and predominantly receives clean air masses from the Atlantic Ocean. As such, observations on the West coast of Ireland have been used as a European reference for transboundary air pollution, e.g., the Mace Head Atmospheric Research Station has been used as a reference site for many pollutants (e.g., Derwent et al., 2007). The three lake catchments used in
The filter papers were analysed for the presence of mf using a stereomicroscope (Leica EZ4W with EZ4W0170 camera) following a five criteria visual identification method modified from Norén (2007) and Windsor et al. (2018). It has been shown that identification of mf according to standardized criteria in connection with strict and conservative examination reduces the possibility of misidentification (Norén, 2007). Further, Löder and Gerdts (2015) demonstrated that for
B. Roblin, J. Aherne / Science of the Total Environment 715 (2020) 136973
3
Table 1 Site description, including coordinates, elevation (EL), long-term average annual air temperature (AT) and annual rainfall (AP) taken from the nearest meteorological station (URL: www. met.ie), and lake surface water concentrations for non-marine sulphate and nitrate during summer 2018 (markers of anthropogenic air pollutant emissions) for the three study catchments. Lake catchment
Latitude
Longitude
Decimal degrees Glendalough Lough Maumwee Lough Veagh
53.00281 53.47672 55.03822
−6.36806 −9.54092 −7.97269
EL
AT
AP
Sulphate −1
m ASL
°C
mm year
μeq L
133 50 43
9.7 10.5 9.9
754 1228 1093
62.7 52.2 55.7
particles N 0.5 mm, visual analyses are suitable for identification. The five criteria were: (i) the fibre is unnaturally coloured (blue, red, green, purple, black, grey) compared with other particles/detritus; (ii) the fibre appears homogenous in material and texture with no visible cell structure or offshoots and is a consistent width throughout its entire length; (iii) the fibre remains intact and is not brittle when compressed, tugged or poked with fine tweezers; (iv) the fibre has a shiny or glossy appearance; and (v) there is limited fraying with no similarities to natural fibres (see Supporting information Table SI-1). It is recommended that at least two of the criteria be met for a fibre to be classified as a microplastic (Windsor et al., 2018). Previous studies have classified all fibres not stained by Rose Bengal as ‘microplastic’ (Liebezeit and Liebezeit, 2014), while others have chosen to use the more general term ‘anthropogenic debris’ (Kosuth et al., 2018). In the current study, non-stained fibres that met two of the criteria were classified as anthropogenic mf; however, the proportion of fibres that met three, four and five criteria were also recorded, with the assumption that fibres that met four–five criteria were more likely plastic. Each mf (that meet two criteria) was photographed and its length was measured using ImageJ processing software (see Supporting information Table SI-2 and Fig. SI-3). It is recognised that only spectroscopic analysis (Fourier Transform infrared (FT-IR) or Raman spectroscopy) can provide unambiguous proof of the synthetic nature of the
−1
Nitrate μeq L−1 15.9 5.6 7.4
non-stained fibres. A small number of fibres were analysed by Raman spectroscopy in the current study (see Supporting information Fig. SI4). 2.5. Quality control and data analysis Throughout sample processing and analysis, procedural open-air blanks were used to determine the amount of potential contamination; open-air and digestion (process) blanks were used during filtering, digesting and oven drying. Digestion blanks were completed by using filtered B-pure™ in place of the sample media during the digestion process. Triplicate B-pure™ water blanks (1 L) were initially vacuum filtered and analysed following the same method as the moss samples to determine the level of mf contamination; the average number of mf in B-pure™ blanks was 11.4 mf L−1 (coefficient of variation of 112%). As such, all B-pure™ water was filtered (Fisherbrand G6: 1.6 μm) prior to use for cleaning and extraction (use in FE(II) solution and Rose Bengal) to avoid potential contamination. Further, during mf extraction (digesting and filtering), samples were covered with aluminium foil to prevent airborne contamination (following Dris et al., 2016; Koelmans et al., 2019; Wright et al., 2019), and all equipment was rinsed with filtered B-pure™ water prior to use. Peroxide blanks (1 L in total) were also vacuum filtered and analysed following the same method as the moss samples to determine the level of mf contamination. Finally, 100% cotton clothes were worn during sample collection, and 100% cotton laboratory coats were worn when extracting and analysing the samples. Where possible the analysis adhered to quality criteria as identified by Koelmans et al. (2019). The number of mf per g (mf g−1) dry moss was calculated using the total mass of moss for each site (which included the fourth digestion and residual fibres in the sampling jar). The coefficient of variation (or relative standard deviation) was used to assess the spread in triplicate 1 g samples. The number of mf per g of dry moss were scaled to atmospheric deposition using published values for the biomass of moss, i.e., 2 kg dry weight m−2 (Forman, 1969; Singh et al., 2005). The longterm atmospheric source regions for each site was evaluated using source-receptor trajectory rose plots (arrival height of 850 hPa) based on two-day back trajectories estimated every 6 h during the period 1989–2009 (see Supporting information Fig. SI-2). Further, the water − concentrations of non-marine sulphate (SO2− 4 ) and nitrate (NO3 ) in each lake during summer 2018 (Table 1) were used to determine the anthropogenic atmospheric influence on the catchments, due to their use as markers for anthropogenic air pollution emissions. 3. Results
Fig. 1. Location of moss (Hylocomium splendens) sampling sites at three lake catchments monitored under ICP Waters: Glendalough, Lough Maumwee and Lough Veagh.
In total there were 28 filter blanks used to estimate the potential contamination of mf from open-air, water, H2O2 and digestion exposure. The average contamination was approximately 0.6 mf g−1 across all sites, i.e., b2.5 mf per site. Only five fibres were observed across all the open-air blanks (n = 20); the largest source of contamination was the unfiltered H2O2, which had 5 mf L−1 (variation between replicates of 40%). The contamination observed for the digestion blanks (n = 3) was 0.33 mf per sample. Given the overall low number, observations were not corrected for contamination in the current study.
4
B. Roblin, J. Aherne / Science of the Total Environment 715 (2020) 136973
Anthropogenic mf were observed in all moss samples (e.g., Supporting information Fig. SI-3) across the three study sites (Table 1); in total 300 mf were recorded across the three sites, ranging from 56 at Lough Maumwee to 162 at Glendalough (Table 2). The average number per site was 24 mf g−1 dry moss (Table 2). The ranged in triplicate moss (1 g) samples was 13–34 mf g−1 at Glendalough, 6–19 mf g−1 at Lough Maumwee, and 8–33 mf g−1 at Lough Veagh (see Supporting information Table SI-2). Glendalough had the least variation between triplicate samples with a coefficient of variation of 46% (Table 2) compared with Lough Maumwee (60%) and Lough Veagh (85%). Given the wide variation in triplicates, larger moss samples potentially provide a more accurate estimate of mf deposition. The length of anthropogenic mf ranged from 0.03–30.25 mm (Fig. 2; see Supporting information Table SI-2) with the longest at each of the sites at 30.25 mm (Glendalough), 3.94 mm (Lough Maumwee) and 4.31 mm (Lough Veagh). The average size of mf was 1.02 mm across the three sites (Table 2), ranging from 0.76 mm (Lough Maumwee) to 1.20 mm (Glendalough). Microfibres observed on moss were predominately b0.8 mm (65%), whereas mf N2 mm only made up 10% (Fig. 2). The coefficient of variation in mf length for the triplicate (1 g) samples ranged from 31% (Lough Veagh) to 42% (Lough Maumwee). To some extent, the most remote site (Lough Maumwee) has the lowest number of fibres and the smallest length of fibre (Table 2). The atmospheric deposition of mf across the three sites was estimated to be ~47,700 mf m−2 (Table 2). Glendalough had the highest estimated deposition at 58,900 mf m−2 followed by Lough Veagh (48,000 mf m−2) and Lough Maumwee (30,600 mf m−2). The proportion of anthropogenic mf that met three or more of the visual assessment criteria, was 70% (three criteria), 27% (four), and 13% met all five criteria (Table 3), suggesting that 13–27% of anthropogenic mf were plastic. Accordingly, the average deposition of plastic mf was estimated to be 6200–12,900 mf m−2. The indicators of anthropogenic atmospheric pollutant deposition (Table 1), non-marine sulphate and nitrate, showed a similar pattern (site ranking) to the anthropogenic mf results (i.e., lowest to highest) Lough Maumwee, Lough Veagh and Glendalough (Table 2); Glendalough had higher concentrations of sulphate and nitrate (62.7 μeq L−1 and 15.9 μeq L−1) compared with Lough Maumwee −1 −1 (52.2 μeq SO2− and 5.6 μeq NO− ). Similarly, the dominant air 4 L 3 L source region to the lakes (i.e., Republic of Ireland and Great Britain), showed a similar pattern to the mf results, i.e., Glendalough had the highest proportion of air from anthropogenic source regions. The correspondence between the number of mf, level of anthropogenic pollutants and air source region, suggests that mf may be subject to longrange atmospheric transport. 4. Discussion Microfibres were observed in all moss samples collected from three lake catchments located in rural regions. The ability of moss to entrap and retain microscopic particles implies that it is a reliable biomonitor of atmospheric mf deposition. Nonetheless, few studies have evaluated moss as a biomonitor for mf; one recent study evaluated the Table 2 The number of microfibres (mf), number per mass (coefficient of variation between triplicates), estimated deposition and average length of mf (coefficient of variation between triplicate 1 g samples) at the three study sites (total mass of moss digested is also shown). Site (mass of moss)
Glendalough (5.50 g) Lough Maumwee (3.66 g) Lough Veagh (3.41 g) Total/average (12.57 g) a
effectiveness of the aquatic moss Sphagnum palustre L. as a biomonitor of microplastics in freshwater environments (Capozzi et al., 2018). Contamination is a concern when dealing with mf. The average contamination was approximately 0.6 mf g−1 across all sites, i.e., b2.5 mf per site. Only five fibres were observed across all the open-air blanks (n = 20); the largest source of contamination was the unfiltered H2O2, which had 5 mf L−1 (variation between replicates of 40%). Given the overall low number, the observation mf in moss samples were assumed to reflect atmospheric deposition. Average atmospheric deposition of mf was estimated to be ~47,700 mf m−2 across the three lake catchments, based on published estimates for the biomass of moss (Table 2). However, moss biomass can vary greatly by site and species of moss; as such, further measurements are needed to accurately scale-up observations on moss to regional deposition. The living green portion of Hylocomium splendens (collected in this study) is considered to represent the last 2–3 years of growth; as such, the estimated deposition may represent a cumulative 2–3 years of deposition. Nonetheless, estimated mf deposition in the current study was similar in magnitude to previous studies that evaluated deposition, e.g., annual atmospheric deposition of mf in in Paris (~30,000 mf m−2 [n = 2]), France, Dongguan city (~72,000 mf m−2 [n = 3]; estimated from three months), China, Nottingham (~27,000 mf m−2 [n = 4]), England, and the Pyrenees mountains (~16,000 mf m−2 [n = 1]; estimated from five months), France (Dris et al., 2016; Cai et al., 2017; Stanton et al., 2019; Allen et al., 2019). The average length of mf observed in this study was 1.02 mm, with ~40% shorter than 0.4 mm (Fig. 2); in contrast, in urban Paris and Dongguan ~40–45% of the observed mf were shorter than 0.6–0.7 mm (Dris et al., 2016; Cai et al., 2017). In the current study, there was a higher proportion of shorter mf at sites more remote from urban centres, e.g., Glendalough, which is on east coast of Ireland and closest to a large population centre (b50 km from Dublin), had the longest fibres (1.20 mm). In contrast, Lough Maumwee, which is more strongly influenced by Atlantic air currents, had the shortest fibres (0.76 mm), suggesting that smaller fibres are more likely to be transported in the atmosphere and make up a higher proportion of the total number of fibres at more remote sites. Further, the number of anthropogenic mf per site was consistent with the level of anthropogenic pollutants and source-receptor analysis, i.e., the study sites had an anthropogenic atmospheric influence in the order of Glendalough N Lough Veagh N Lough Maumwee, which was consistent with the total number and average length of mf observed at the sites (Tables 1 and 2). On average, only 13% of the observed mf passed all five identification criteria and 27% passed four criteria per site (Table 3). In the current study, it was assumed that mf that met four or five identification criteria, had a greater likelihood of being plastics, i.e., 13–27% of mf were microplastics. This range was similar to previous studies, e.g., the proportion of plastic mf in atmospheric deposition was estimated to be 23% in Dongguan City, China, and 29% in urban Paris, France, based on FT-IR spectroscopy (Dris et al., 2016; Cai et al., 2017). It is difficult to unambiguously visually-discriminate all potential microplastic particles; error rates of visual sorting are reported to range from 20% (Eriksen et al., 2013) to 70% (Hidalgo-Ruz et al., 2012) and increase with decreasing particle size. Further, with respect to mf, Stanton et al. (2019) suggest that airborne fibre populations are largely dominated (N90%) by ‘natural’ textile, rather than microplastic fibres, which is consistent with the current study (13–27%).
Microfibres
Microfibres
Depositiona
Average length
5. Conclusions
n
n g−1
mf m−2
mm
162 56 82 300
29.5 (46%) 15.3 (60%) 24.0 (85%) 23.9
58,900 30,600 48,000 47,700
1.20 (36%) 0.76 (42%) 0.83 (31%) 1.02
Anthropogenic mf were observed in moss samples collected from remote lake catchments in Ireland; the magnitude and length of mf were similar to previous atmospheric studies. These preliminary results suggest that bryophytes may be a suitable biomonitor for the atmospheric deposition of mf. Furthermore, the relative magnitude of air from anthropogenically impacted regions, as indicated by trajectory analysis
Based on a biomass of 2 kg dry weight m−2.
B. Roblin, J. Aherne / Science of the Total Environment 715 (2020) 136973
5
Fig. 2. Size distribution (μm) of anthropogenic microfibres (n = 300) extracted from moss samples collected at three ICP Waters lake catchments (see Fig. 1).
and lake chemistry analysis, was consistent with the number of anthropogenic mf observed at each site, suggesting that mf may be subject to long-range atmospheric transport.
Author contributions BR conducted the field sampling, microfibre extractions, microscopy and microfibre identification. BR and JA designed the study, carried out the data analysis, wrote the main manuscript and prepared the figures.
Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements We gratefully acknowledge the Irish Environmental Protection Agency for funding this study (2016-CCRP-MS.43) and thank the National Parks and Wildlife Service, Inland Fisheries and the Corrnamona Angling Club for site access and logistical support. Finally, we would like to thank Hazel Cathcart for field assistance. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.scitotenv.2020.136973. Table 3 The percent of anthropogenic fibres that met three, four and five of the visual identification criteria per site (Glendalough, Lough Maumwee and Lough Veagh). The average across the three sites along with the average length is also given. Site
3 of 5 criteria
4 of 5 criteria
5 of 5 criteria
Glendalough Lough Maumwee Lough Veagh Average Length (mm)
69% 71% 71% 70% 1.00
27% 23% 28% 27% 1.01
15% 14% 10% 13% 1.92
References Aceto, M., et al., 2003. The use of mosses as environmental metal pollution indicators. Chemosphere 50, 333–342. Adamo, P., Giordano, S., Naimo, D., Bargagli, R., 2008. Geochemical properties of airborne particulate matter (PM10) collected by automatic device and biomonitors in a Mediterranean urban environment. Atmos. Environ. 42, 346–357. Allen, S., et al., 2019. Atmospheric transport and deposition of microplastics in a remote mountain catchment. Nat. Geosci. 12, 339–344. Barrows, A.P., Cathey, S., Peterson, C., 2018. Marine environment microfiber contamination: global patterns and the diversity of microparticle origins. Environ. Pollut. 237, 275–284. Berg, T., Røyset, O., Steinnes, E., 1995. Moss (Hylocomium splendens) used as biomonitor of atmospheric trace element deposition: estimation of uptake efficiencies. Atmos. Environ. 29, 353–360. Bergmann, M., Mützel, S., Primpke, S., Tekman, M., Trachsel, J., Gerdts, G., 2019. White and wonderful? Microplastics prevail in snow from the Alps to the Arctic. Sci. Adv. 5 (8), EAAX1157. Bowman, J., 1986. Precipitation Characteristics and the Chemistry and Biology of Poorly Buffered Irish Lakes: A Western European Baseline for ‘Acid Rain’ Impact Assessment. An Foras Forbartha, Dublin WR/G14. Bowman, J., 1991. Acid Sensitive Surface Waters in Ireland. Environmental Research Unit, Dublin, Ireland, p. 321. Cago, J., Carretero, O., Filgueiras, A., Vinas, L., 2018. Synthetic microfibers in the marine environment: a review on their occurrence in seawater and sediments. Mar. Pollut. Bull. 127, 365–376. Cai, L., et al., 2017. Characteristic of microplastics in the atmospheric fallout from Dongguan city, China: preliminary research and first evidence. Environ. Sci. Pollut. Res. 24, 24928–24935. Capozzi, F., Carotenuto, R., Giordano, S., Spagnuolo, V., 2018. Evidence on the effectiveness of mosses for biomonitoring of microplastics in fresh water environment. Chemosphere 205, 1–7. Clough, W., 1975. The deposition of particles on moss and grass surfaces. Atmos. Environ. 9, 1113–1119. Cole, M., Lindeque, P., Halsband, C., Galloway, T.S., 2011. Microplastics as contaminants in the marine environment: a review. Mar. Pollut. Bull. 62, 2588–2597. Cowden, P., Aherne, J., 2019. Assessment of atmospheric metal deposition by moss biomonitoring in a region under the influence of a long standing active aluminium smelter. Atmos. Environ. 201, 84–91. Derwent, R., Simmonds, P., Manning, A., Spain, T., 2007. Trends over a 20-year period from 1987 to 2007 in surface ozone at the atmospheric research station, Mace Head, Ireland. Atmos. Environ. 41, 9091–9098. Dris, R., et al., 2015. Microplastic contamination in an urban area: a case study in Greater Paris. Environ. Chem. 12 (2015), 592–599. Dris, R., Gasperi, J., Saad, M., Mirande, C., Tassin, B., 2016. Synthetic fibers in atmospheric fallout: a source of microplastics in the environment? Mar. Pollut. Bull. 104, 290–293. Eriksen, M., et al., 2013. Microplastic pollution in the surface waters of the Laurentian Great Lakes. Mar. Pollut. Bull. 77, 177–182. Forman, R., 1969. Comparison of coverage, biomass, and energy as measures of standing crop of bryophytes in various ecosystems. Bull. Torrey. Bot. Club 96, 582. Halleraker, J., et al., 1998. Reliability of moss (Hylocomium splendens and Pleurozium schreberi) as a bioindicator of atmospheric chemistry in the Barents region: interspecies and field duplicate variability. Sci. Total Environ. 218, 123–139.
6
B. Roblin, J. Aherne / Science of the Total Environment 715 (2020) 136973
Harmens, H., et al., 2010. Mosses as biomonitors of atmospheric heavy metal deposition: spatial patterns and temporal trends in Europe. Environ. Pollut. 158, 3144–3156. Harmens, H., et al., 2011. Nitrogen concentrations in mosses indicate the spatial distribution of atmospheric nitrogen deposition in Europe. Environ. Pollut. 159, 2852–2860. Harmens, H., Foan, L., Simon, V., Mills, G., 2013. Terrestrial mosses as biomonitors of atmospheric POPs pollution: a review. Environ. Pollut. 173, 245–254. Herrera, A., et al., 2018. Novel methodology to isolate microplastics from vegetal-rich samples. Mar. Pollut. Bull. 129 (1), 61–69. Hidalgo-Ruz, V., Gutow, L., Thompson, R.C., Thiel, M., 2012. Microplastics in the marine environment: a review of the methods used for identification and quantification. Environ. Sci. Technol. 46, 3060–3075. Horton, A., Dixon, S., 2018. Microplastics: an introduction to environmental transport processes. Wiley Interdiscip. Rev. Water 5, e1268. Horton, A.A., Walton, A., Spurgeon, D.J., Lahive, E., Svendsen, C., 2017. Microplastics in freshwater and terrestrial environments: evaluating the current understanding to identify the knowledge gaps and future research priorities. Sci. Total Environ. 586, 127–141. International Cooperation Programme Vegetation (ICPV), 2015. Monitoring of Atmospheric Deposition of Heavy Metals, Nitrogen and POPs in Europe Using Bryophytes. Monitoring Manual. Koelmans, A.A., Nor, N.H.M., Hermsen, E., Kooi, M., Mintenig, S.M., De France, J., 2019. Microplastics in freshwaters and drinking water: critical review and assessment of data quality. Water Res. 155, 410–422. Kosuth, M., Mason, S.A., Wattenberg, E.V., 2018. Anthropogenic contamination of tap water, beer, and sea salt. PLoS One 13, e0194970. Liebezeit, G., Liebezeit, E., 2014. Synthetic particles as contaminants in German beers. Food Addit. Contam. Part A 31, 1574–1578. Löder, M.G.J., Gerdts, G., 2015. In: Bergmann, M., Gutow, L., Klages, M. (Eds.), Marine Anthropogenic Litter. Springer, Cham, pp. 201–227. Masura, J., Baker, J., Foster, G., Arthur, C., 2015. Laboratory methods for the analysis of microplastics in the marine environment: recommendations for quantifying synthetic particles in waters and sediments. NOAA Technical Memorandum NOSOR&R-48. Norén, F., 2007. Small Plastic Particles in Coastal Swedish Waters. KIMO, Sweden. Olmstead, E., Aherne, J., 2019. Are tissue concentrations of Hylocomium splendens a good predictor of nitrogen deposition? Atmos. Pollut. Res. 10, 80–87.
Peng, J., Wang, J., Cai, L., 2017. Current understanding of microplastics in the environment: occurrence, fate, risks, and what we should do. Integr. Environ. Assess. Manag. 13, 476–482. Rühling, A., Tyler, G., 1968. An ecological approach to the lead problem. Bot. Notiser 121, 321–342. Rühling, Å., Tyler, G., 1970. Sorption and retention of heavy metals in the woodland moss Hylocomium splendens (Hedw.) Br. et Sch. Oikos 21, 92. Schintu, M., Cogoni, A., Durante, L., Cantaluppi, C., Contu, A., 2005. Moss (Bryum radiculosum) as a bioindicator of trace metal deposition around an industrialised area in Sardinia (Italy). Chemosphere 60, 610–618. Singh, M., et al., 2005. Preliminary estimation of bryophyte biomass and carbon pool from three contrasting different vegetation types. Cereal Research Communications 33, 267–270. Stanton, T., Johnson, M., Nathanail, P., MacNaughtan, W., Gomes, R., 2019. Freshwater and airborne textile fibre populations are dominated by ‘natural’, not microplastic, fibres. Sci. Total Environ. 666, 377–389. Suchara, I., et al., 2011. The performance of moss, grass, and 1- and 2-year old spruce needles as bioindicators of contamination: a comparative study at the scale of the Czech Republic. Sci. Total Environ. 409, 2281–2297. Wagner, M., et al., 2014. Microplastics in freshwater ecosystems: what we know and what we need to know. Environ. Sci. Eur. 26, 1–9. Wesch, C., et al., 2017. Assuring quality in microplastic monitoring: about the value of clean-air devices as essentials for verified data. Sci. Rep. 7. Wilkins, K., Aherne, J., 2015. Isothecium myosuroides and Thuidium tamariscinum mosses as bioindicators of nitrogen and heavy metal deposition in Atlantic oak woodlands. Ann. Bot. (Roma) 5, 71–78. Windsor, F., Tilley, R., Tyler, C., Ormerod, S., 2018. Microplastic ingestion by riverine macroinvertebrates. Sci. Total Environ. 646, 68–74. Wright, S.L., Ulke, J., Font, A., Chan, K.L.A., Kelly, F.J., 2019. Atmospheric microplastic deposition in an urban environment and an evaluation of transport. Environ. Int. 105411. Zhang, K., et al., 2016. Microplastic pollution of lakeshore sediments from remote lakes in Tibet plateau, China. Environ. Pollut. 219, 450–455. Zhao, S., Zhu, L., Wang, T., Li, D., 2014. Suspended microplastics in the surface water of the Yangtze Estuary System, China: first observations on occurrence, distribution. Mar. Pollut. Bull. 86, 562–568.