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Microplastics in freshwater ecosystems: what we know and what we need to know

Microplastics in freshwater ecosystems: what we know and what we need to know Background: While the use of plastic materials has generated huge societal benefits, the ‘plastic age’ comes with downsides: One issue of emerging concern is the accumulation of plastics in the aquatic environment. Here, so-called microplastics (MP), fragments smaller than 5 mm, are of special concern because they can be ingested throughout the food web more readily than larger particles. Focusing on freshwater MP, we briefly review the state of the science to identify gaps of knowledge and deduce research needs. State of the science: Environmental scientists started investigating marine (micro)plastics in the early 2000s. Today, a wealth of studies demonstrates that MP have ubiquitously permeated the marine ecosystem, including the polar regions and the deep sea. MP ingestion has been documented for an increasing number of marine species. However, to date, only few studies investigate their biological effects. The majority of marine plastics are considered to originate from land-based sources, including surface waters. Although they may be important transport pathways of MP, data from freshwater ecosystems is scarce. So far, only few studies provide evidence for the presence of MP in rivers and lakes. Data on MP uptake by freshwater invertebrates and fish is very limited. Knowledge gaps: While the research on marine MP is more advanced, there are immense gaps of knowledge regarding freshwater MP. Data on their abundance is fragmentary for large and absent for small surface waters. Likewise, relevant sources and the environmental fate remain to be investigated. Data on the biological effects of MP in freshwater species is completely lacking. The accumulation of other freshwater contaminants on MP is of special interest because ingestion might increase the chemical exposure. Again, data is unavailable on this important issue. Conclusions: MP represent freshwater contaminants of emerging concern. However, to assess the environmental risk associated with MP, comprehensive data on their abundance, fate, sources, and biological effects in freshwater ecosystems are needed. Establishing such data critically depends on a collaborative effort by environmental scientists from diverse disciplines (chemistry, hydrology, ecotoxicology, etc.) and, unsurprisingly, on the allocation of sufficient public funding. Keywords: Chemistry; Ecotoxicology; Environmental quality; Litter; Microplastics; Monitoring; Plastics; Polymers; Review; Water framework directive * Correspondence: wagner@bio.uni-frankfurt.de Department of Aquatic Ecotoxicology, Goethe University Frankfurt am Main, Max-von-Laue-Str. 13, Frankfurt 60438, Germany Full list of author information is available at the end of the article © 2014 Wagner et al.; licensee Springer. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. Wagner et al. Environmental Sciences Europe 2014, 26:12 Page 2 of 9 http://www.enveurope.com/content/26/1/12 Background however, focus almost exclusively on marine plastic debris. Microplastics are freshwater contaminants of emerging However, we argue that microplastics are also freshwater concern contaminants of emerging concern.Thisis supported by Among the multiple human pressures on aquatic ecosys- three arguments. First, although data is scarce, MP are tems, the accumulation of plastic debris is one of the present in freshwater ecosystems. Second, MP contain most obvious but least studied. While plastics generate and adsorb micropollutants and pathogens. Third, labora- remarkable societal benefits [1], there are downsides to tory studies demonstrate that marine organisms ingest our ‘plastic age’. Durability, unsustainable use, and in- MP and suffer adverse effect. While data on freshwater appropriate waste management cause an extensive accu- species is scarce, there is no reason to suppose that they mulation of plastics in natural habitats [2]. In the marine remain unaffected. Thus, concerns about the impact of environment, plastics of various size classes and origins MP on freshwater ecosystems are legitimate and should are ubiquitous and affect numerous species that become receive more scientific attention. entangled in or ingest plastics [3]. Under environmental conditions, larger plastic items State of the science: focus on marine microplastics degrade to so-called microplastics (MP), fragments typ- So far, scientific efforts focus on marine MP, and studies ically smaller than 5 mm in diameter (see Table 1 for on their abundance and effects become increasingly avail- further information). Besides these degradation products able. Because of its high mobility, plastic debris has prac- (secondary MP), MP can also be produced as such (pri- tically permeated the global marine environment [14,15], mary MP). For instance, MP are intentionally used as including the polar regions [2], mid-ocean islands [16], resin pellets (raw material for the production of plastic and the deep sea [17]. Because of their specific hydrol- products) or as ingredient of personal care products ogy, the large oceanic gyres are hot spots of plastic pollu- (e.g., peelings and shower gels). tion (colloquially termed ‘garbage patches’), accumulating MP are of special concern since their bioaccumulation buoyant plastic debris. Here, the plastic abundance often potential increases with decreasing size. MP may be exceeds that of zooplankton [18-21]. With respect to ingested by various organisms ranging from plankton Europe's regional seas, MP have been reported for the and fish to birds and even mammals, and accumulate Baltic, North, and Mediterranean Sea [22-25]. throughout the aquatic food web [4]. In addition, plastics Most of the studies investigate neustonic and pelagic contain a multitude of chemical additives [5] and adsorb MP. However, MP are also present in sediments and have organic contaminants from the surrounding media [6]. been detected on the shorelines and seafloors of six conti- Since these compounds can transfer to organisms upon nents [15,26,27] with typical concentrations ranging from −1 ingestion, MP act as vectors for other organic pollutants 1to 100 items kg [28]. A Belgian study reports a max- −1 [7] and are, therefore, a source of wildlife exposure to imum of 400 items kg in coastal harbor sediments [29]. these chemicals [8,9]. Higher concentrations were reported in a Dutch study −1 Accordingly, MP are considered an emerging global with 770 and 3,300 items kg dry weight sediment in the issue by various experts [10,11] and international institu- Wadden Sea and the Rhine estuary, respectively [30]. Al- tions [12,13]. These concerns and the public interest, though abundant ubiquitously, the spatial distribution of Table 1 Classification of environmental (micro)plastics Category Description Classification Environmental plastics are a very heterogeneous group of litter that can be characterized by various descriptors. In the literature, they are frequently stratified according to size, origin, shape, polymer type, and color. So far, there is no common classification system. Recently, the European MSFD Working Group on Good Environmental Status (WG-GES) provided a ‘Monitoring Guidance for Marine Litter in European Seas’ [76], which represents an important step towards a standardized sampling and monitoring of marine microplastics. Size The WG-GES defines size classes for plastic litter as follows: macroplastics (>25 mm), mesoplastics (5 to 25 mm), large microplastics (1 to 5 mm), and small microplastics (20 μm to 1 mm). Accordingly, items smaller than 20 μm will classify as nanoplastics. Origin Microplastics can also be categorized according to its origin: Primary microplastics are produced as such, for instance as resin pellets (raw materials for plastic products) or as additives for personal care products (e.g., shower gels and peelings). Secondary microplastics are degradation products of larger plastic items, which are broken down by UV radiation and physical abrasion to smaller fragments. Polymers The polymer type of environmental (micro)plastics can be determined by Fourier transformed infrared spectroscopy (FT-IR) or Raman spectroscopy. In concordance to global production rates, high- and low-density polyethylene (HD/LD-PE), polyethylene terephthalate (PET), polypropylene (PP), polystyrene (PS), and polyvinyl chloride (PVC) are the most common polymers found in the environment. In addition, polyamide fibers (nylon) from fishing gears are frequent. Shape The shape can be described according to the main categories: fragments (rounded, angular), pellets (cylinders, disks, spherules), filaments (fibers), and granules [76]. Wagner et al. Environmental Sciences Europe 2014, 26:12 Page 3 of 9 http://www.enveurope.com/content/26/1/12 MP in the marine environment is very heterogeneous Lakes, MP here consisted mainly of low-density poly- [14]. This might be partly due to differences in method- mers (polystyrene (PS), polyethylene (PE), and polypro- ology [28]. pylene (PP)). Field reports on detrimental interactions of plastics Moore et al. [45] provide the first, non-peer-reviewed with biota (e.g., entanglement) are manifold [4]. How- report on MP in rivers. In three Californian rivers, they −3 ever, only about a dozen studies have investigated MP found, on average, 30 to 109 items m . The midstream −3 uptake and effects under laboratory conditions, includ- of the Los Angeles River carried 12,000 items m and −1 ing two studies on freshwater species (literature search will discharge > 1 billion MP items day into the Pacific on ISI Web of Science, search term ‘microplastic*’, man- Ocean. Although very limited, this data indicates that ual filtering). With nine of these papers published since rivers transport relevant amounts of MP. 2012, this is a very recent area of research. The ingestion According to a recent study, the same is true for the of MP by marine invertebrates has been demonstrated in second largest European rivers: Lechner et al. [46] used the laboratory for a broad spectrum of marine species: stationary driftnets and visual inspection to monitor zooplankton [31-33], the lugworm Arenicola marina [34], plastic debris in the Austrian Danube. The authors re- the Blue mussel Mytilus edulis [35-37], and the sandhop- port approximately 900 (2010) and 50 (2012) plastic −3 per Talitrus saltator [38]. M. edulis is the only invertebrate items 1,000 m in the size class of 0.5 to 50 mm. In a in which the transfer of MP from the digestive tract to tis- worst-case scenario, the Danube would discharge 4.2 t −1 −1 sue has been studied and documented [35,36]. plastics day and 1,500 t plastics year to the Black Data on the effects of MP exposure is limited. For zoo- Sea. The latter is more than the total plastic load of the plankton, a reduced algal feeding has been observed [31]. whole North Atlantic Gyre [47]. Lechner et al. provide MP increased the mortality and decreased the fertility in first evidence that large rivers transport significant copepods [32]. In the lugworm, MP reduced the weight amounts of (micro)plastics and thus contribute substan- and feeding and increased the bioaccumulation of plastic- tially to the marine plastics pollution. associated polychlorinated biphenyls (PCBs) [34]. Reduced Because data on the presence of MP in river sediments filtering activity and histological changes as response to is lacking, the Federal Institute of Hydrology and the inflammation have been reported for M. edulis [36,37], al- Goethe University carried out a small, exploratory study though another study did not find significant effects [35]. with sediments from the rivers Elbe, Mosel, Neckar, and In the only study with marine vertebrates, the common Rhine (Germany). Using density separation and visual −1 goby Pomatoschistus microps was exposed to MP and pyr- inspection, we found 34 to 64 MP items kg dry weight, ene [39]. MP delayed the pyrene-induced mortality but in- with the River Rhine containing the highest load. Plastic duced several toxicity biomarkers. In addition, two recent fragments accounted for 60% of the total MP; the remaining studies demonstrate the trophic transfer of MP along the particles were synthetic fibers (Figure 1). Thus, as is the case marine food web from meso- to macrozooplankton [33] for marine and estuarine sediments, river and lake sedi- and from mussels to crabs [40]. ments may be sinks for MP, deserving further investigation. Discussion Sources of microplastics Presence of microplastics in freshwater ecosystems To date, the sources of marine MP are still not very well Despite of the wealth of data on marine MP, to date, characterized. A rough estimation predicts that 70% to only a handful of studies investigate MP in a freshwater 80% of marine litter, most of it plastics, originate from in- context. MP have been detected in the surface waters of land sources and are emitted by rivers to the oceans [12]. the Laurentian Great Lakes [41]. The average abundance Potential sources include wastewater treatment plants −2 in the neuston was 43,000 items km , with a hotspot (WWTPs), beach litter, fishery, cargo shipping, and har- near metropolitan areas, which may represent important bors [12,23,25,29,48]. Although data is so far unavailable, sources. runoff from industrial plastic production sites may be an Three studies report the occurrence of MP in the sedi- additional source. Taken together, most marine studies ments of lakes. Zbyszewski and Corcoran [42] found 0 to tentatively refer to inland waters as relevant sources (in- −2 34 plastic fragments m on the shorelines of Lake Huron deed they are rather transport pathways), while actual data (Canada). Here, MP accumulation may be attributed to is still scarce. the lake's currents and nearby plastic manufacturers. Ex- Inland sources of MP have not been investigated thor- tending their shoreline monitoring to the Lakes Erie and oughly. In analogy to the marine systems, major contrib- −2 St. Clair, Zbyszewski et al. [43] report 0.2 to 8 items m . utors will likely include WWTPs and runoff from urban, Sampling two beaches of Lake Garda (Italy), Imhof et al. agricultural, touristic, and industrial areas, as well as −2 [44] found 100 and 1,100 MP items m at the southern shipping activities. Another potential source is sewage and northern shores, respectively. Similar to the Great sludge that typically contains more MP than effluents Wagner et al. Environmental Sciences Europe 2014, 26:12 Page 4 of 9 http://www.enveurope.com/content/26/1/12 Figure 1 Microplastics in sediments from the rivers Elbe (A), Mosel (B), Neckar (C), and Rhine (D). Note the diverse shapes (filaments, fragments, and spheres) and that not all items are microplastics (e.g., aluminum foil (C) and glass spheres and sand (D), white arrowheads). The white bars represent 1 mm. [49]. Sewage sludge is still frequently used for landfilling Microplastics as vector for other contaminants and as fertilizer in agriculture, and surface runoff may Due to their large surface-to-volume ratio and chemical transfer MP to rivers and lakes and ultimately river ba- composition, MP accumulate waterborne contaminants in- sins and the sea. Washing clothes [26] and personal care cluding metals [53] and persistent, bioaccumulative, and products [50] are sources of MP in WWTPs. Since the re- toxic compounds (PBTs) [54]. A review on the relationship tention capacity of conventional wastewater treatment pro- between plastic debris and PBTs (e.g., PCBs and DDT) has cesses appears to be limited [14], a characterization of MP been published recently [55], and a number of studies exist emission by WWTPs and other sources is urgently needed for polycyclic aromatic hydrocarbons (PAHs) [56-61]. How- to understand where freshwater MP is coming from. ever, there is a lack of information on other important con- taminants like pharmaceuticals and endocrine-disrupting Impact of microplastics on freshwater species compounds (EDCs). Nonylphenol and bisphenol A have In a field report, Sanchez et al. [51] provide the only data been detected in MP [60,62,63]. Fries et al. [24] detected on MP in freshwater fish so far. They investigated various plastic additives in MP, including some well-known gudgeon (Gobio gobio) caught in 11 French streams and EDCs (e.g., phthalates). In addition, Wagner and Oehlmann found MP in the digestive tract of 12% of the fish. Al- [64,65] demonstrated that plastics leach EDCs. Since the though again very preliminary, this field report shows spectrum of contaminants is different in freshwater and that freshwater species ingest MP. However, the rate of marine systems, the chemical burden of freshwater MP re- MP ingestion in different fish species will certainly de- mains to be studied. pend on their feeding strategy. Rosenkranz et al. [52] The interaction of MP and chemicals has been studied demonstrate that the water flea Daphnia magna rapidly in adsorption-desorption experiments [6,57]. While there ingests MP under laboratory conditions. MP (0.02 and 1 is significant complexity in this interaction, MP may act as mm) appear to cross the gut epithelium and accumulate vector transferring environmental contaminants from in lipid storage droplets. This is of specific concern water to biota. While different modeling studies arrive at because MP infiltrating tissues might induce more se- contrasting conclusions [54,66,67], a recent experimental vere effects. Imhof et al. [44] report the uptake of MP by study demonstrates that fish exposed to contaminants annelids (Lumbriculus variegatus), crustaceans (D. magna sorbed to MP bioaccumulate these compounds and suffer and Gammarus pulex), ostracods (Notodromas monacha), adverse effects (glycogen depletion and histopathological and gastropods (Potamopyrgus antipodarum). While the alterations [68]). However, to date, there are too few stud- available studies demonstrate that a broad spectrum of ies investigating whether MP are indeed vectors that facili- aquatic taxa is prone to MP ingestion, the toxicological ef- tate the transfer of organic contaminants to biota. Because fects remain uninvestigated for freshwater species. a verification of the ‘vector hypothesis’ would have major Wagner et al. Environmental Sciences Europe 2014, 26:12 Page 5 of 9 http://www.enveurope.com/content/26/1/12 ecological implications, it deserves further investigation, In a recent ‘Green paper on a European strategy on plas- especially in a freshwater context. tic waste in the environment, ’ the European Commission addresses the issue as part of a wider review of its waste le- Microplastics as vector for exotic species and pathogens gislation [74]. While the Green Paper focuses on potential Not only the complex mix of chemicals contained in and mitigation strategies for plastic litter at the source, it also sorbed to MP and/or ingestion of MP by biota is a cause expresses ‘particular concern’ about MP. for concern but also microorganisms developing biofilms on MP particles. Only very few studies have been con- Conclusions ducted on this issue with marine ecosystems being the Knowledge gaps and research needs focal point of interest [69-72]. Zettler et al. [72] described The investigation of (micro)plastics in aquatic environ- a highly diverse microbial community (‘plastisphere’) ments is a highly dynamic and interdisciplinary area of attaching plastic marine debris in the North Atlantic. Sev- research covering and bringing together the disciplines eral plastisphere members are hydrocarbon-degrading of oceanography and hydrology as well as environmental bacteria which may potentially influence plastic debris monitoring, modeling, chemistry, and toxicology. In recent fragmentation and degradation. But they also found op- years, this collaborative effort advanced our understanding portunistic (human) pathogens like specific members of of the environmental impact of MP, especially by providing the genus Vibrio dominating plastic particles. Therefore, extensive monitoring data. Ongoing research activities MP can act as a vector for waterborne (human) path- focus, however, almost exclusively on marine MP. ogens influencing the hygienic water quality. The fact Data on freshwater ecosystems is at best fragmentary that the microbial communities on MP are distinct from if not absent. This lack of knowledge hampers a science- surrounding water (only some marine bacteria develop based environmental risk assessment of freshwater MP. biofilms on microplastic particles (e.g., [71,72])) suggests Such assessment is needed to facilitate a societal and that MP serve as a kind of new habitat. Until now, the political discussion at national and European levels on the complex interaction between microorganisms/microbial issue, which, depending on the outcome, will result in communities as a key player in aquatic ecosystems/food mitigation measures eventually. For instance, MP could be webs and MP, especially in freshwater, is poorly under- integrated as descriptor of environmental status in the stood and needs to be further investigated. WFD. However, environmental scientists first need to close the gaps of knowledge with regard to exposure and Microplastics in connection to European water policies hazard of freshwater MP and the associated chemicals. The issue of (micro)plastics connects to several European Based on the current state of the science, the following re- water policies. The European Marine Strategy Framework search needs emerge (Figure 2): Directive (MSFD, 2008/56/EC) addresses the issue of marine litter, including plastics. Here, MP are covered by 1. Monitoring the presence of microplastics in Descriptor 10 of Commission Decision 2010/477/EU, freshwater systems. While few studies on large lakes which defines the good environmental status of mar- and rivers are available, we have no clear picture on ine waters [73]. the magnitude of the plastics pollution in surface In contrast, the Water Framework Directive (WFD, 20/ waters. Generating comprehensive monitoring data 60/EC) applying to European inland waters does not spe- on the abundance of freshwater MP is needed to cifically refer to plastic litter. However, the Member States understand their environmental impact. have the obligation to monitor anthropogenic pressures. 2. Investigating the sources and fate of freshwater Here, MP are promising candidates, especially because microplastics. Currently, we still do not understand they might act as vectors for a wide range of freshwater the behavior of MP in aquatic ecosystems. Based on contaminants. For instance, MP have been shown to con- data on their abundance, modeling approaches are tain the WFD priority substances di(ethylhexyl) phthalate needed to identify hotspots and sinks and quantify (DEHP), nonylphenol, octylphenol, and PAHs (2008/105/ loads. One important aspect of understanding the EC, Annex II). environmental fate is also to identify relevant inland Several other European Directives relate to the potential sources of MP and determine the fragmentation sources of freshwater MP, including the Directives on pack- rates of large plastic debris. aging waste (2004/12/EC), waste (2008/98/EC), landfills 3. Assessing the exposure to microplastics. With (1999/31/EC), urban wastewater (91/271/EEC), sewage evidence coming from marine species, it appears sludge (86/278/EEC), and ship-source pollution (2005/35/ plausible that freshwater organisms will ingest MP, EC). In addition, the Union's chemicals legislation (REACH, too. However, actual data is scarce. Environmental 1907/2006/EC) will apply to plastic monomers and addi- toxicologists need to determine the intake of MP by tives of relevant production volumes. freshwater key species. It will be crucial to Wagner et al. Environmental Sciences Europe 2014, 26:12 Page 6 of 9 http://www.enveurope.com/content/26/1/12 Figure 2 Research aspects with regard to freshwater microplastics. All areas need to be investigated more thoroughly to assess the environmental risk associated with microplastics in freshwater ecosystems. understand which plastic characteristics (size, pollutants is very different. Therefore, it is important material, and shape) promote an uptake and what is to investigate the chemical burden of freshwater MP, the fate of MP in the biota (e.g., excretion, including the absorption/desorption kinetics and the accumulation, and infiltration of tissues). These transfer of chemicals from plastics to biota. aspects need to be studied under laboratory 6. Develop a novel framework for the risk assessment conditions and in the field to determine the actual of microplastics. MP can be direct and indirect exposure. stressors for the aquatic environment: They are 4. Evaluating the biological effects of microplastics contaminants of emerging concern per se and, in exposure. Besides abundance and exposure, the addition, may serve as vectors for invasive species and question whether MP induce adverse effects in for other pollutants. To account for that, the classical organisms is crucial to determine their risk assessment framework needs to be adapted. environmental hazard. In the absence of effect For instance, the mixture toxicity of MP-associated studies on freshwater species, one can only speculate compounds and the modulation of the compounds' on potential sensitive endpoints: Ingested plastic bioavailability need to be integrated. fragments may most likely affect the metabolism (starvation due to decreased energy intake) and There are some challenges in investigating these aspects: induce inflammation (when transferring to tissues). To generate commensurable data on the abundance of Because this is an area of research where the least freshwater MP, harmonized monitoring procedures, in- progress has been made so far, the investigation of cluding sampling, identification, and characterization, are MP effects on marine and freshwater species need to needed. For that, the ‘Monitoring Guidance for Marine be intensified considerably. Litter in European Seas’ developed by the European MSFD 5. Understanding the interaction between microplastics Working Group on Good Environmental Status [76] and other freshwater contaminants. Plastics itself can provides an excellent starting point. The separation of contain and release toxic chemicals (e.g., monomers MP from the sample materials (sediments or suspended or plastic additives [75]). In addition, they can particulate matter) and the confirmation of the plastics' accumulate environmental chemicals from the identity to avoid misclassification is still a very resource- surrounding. This may increase the chemical consuming and biased process (e.g., when visually identi- exposure of the ingesting organism and, thus, toxicity. fying MP in complex samples). Here, sample throughput and accuracy need to be increased. Likewise, we need to The findings on chemicals associated with marine MP (mostly POPs) cannot be transferred to freshwaters improve the capability to detect very small MP in the low because here the spectrum and concentrations of micrometer range. Boosting technological innovation in Wagner et al. Environmental Sciences Europe 2014, 26:12 Page 7 of 9 http://www.enveurope.com/content/26/1/12 the area of MP research (e.g., coupling of microscopy and 4. Wright SL, Thompson RC, Galloway TS: The physical impacts of microplastics on marine organisms: a review. Environ Pollut 2013, spectroscopy to identify very small MP) will help meet 178:483–492. those challenges. 5. Dekiff JH, Remy D, Klasmeier J, Fries E: Occurrence and spatial distribution In conclusion, based on our knowledge on the envir- of microplastics in sediments from Norderney. Environ Pollut 2014, 186:248–256. onmental impact of marine MP, their freshwater coun- 6. 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Environmental Sciences Europe 2014, 26:12 Page 9 of 9 http://www.enveurope.com/content/26/1/12 73. Galgani F, Hanke G, Werner S, De Vrees L: Marine litter within the European Marine Strategy Framework Directive. ICES J Mar Sci 2013, 70:1055–1064. 74. European Commission: Green Paper on a European Strategy on Plastic Waste in the Environment. Brussels: European Commission; 2013. 75. Rochman CM: Plastics and priority pollutants: a multiple stressor in aquatic habitats. Environ Sci Technol 2013, 47:2439–2440. 76. MSFD GES Technical Subgroup on Marine Litter (TSG-ML): Monitoring Guidance for Marine Litter in European Seas, Draft report. Brussels: European Commission; 2013. doi:10.1186/s12302-014-0012-7 Cite this article as: Wagner et al.: Microplastics in freshwater ecosystems: what we know and what we need to know. Environmental Sciences Europe 2014 26:12. 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Copyright © 2014 by Wagner et al.; licensee Springer
Subject
Environment; Environment, general; Pollution, general; Ecotoxicology
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2190-4707
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2190-4715
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10.1186/s12302-014-0012-7
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Abstract

Background: While the use of plastic materials has generated huge societal benefits, the ‘plastic age’ comes with downsides: One issue of emerging concern is the accumulation of plastics in the aquatic environment. Here, so-called microplastics (MP), fragments smaller than 5 mm, are of special concern because they can be ingested throughout the food web more readily than larger particles. Focusing on freshwater MP, we briefly review the state of the science to identify gaps of knowledge and deduce research needs. State of the science: Environmental scientists started investigating marine (micro)plastics in the early 2000s. Today, a wealth of studies demonstrates that MP have ubiquitously permeated the marine ecosystem, including the polar regions and the deep sea. MP ingestion has been documented for an increasing number of marine species. However, to date, only few studies investigate their biological effects. The majority of marine plastics are considered to originate from land-based sources, including surface waters. Although they may be important transport pathways of MP, data from freshwater ecosystems is scarce. So far, only few studies provide evidence for the presence of MP in rivers and lakes. Data on MP uptake by freshwater invertebrates and fish is very limited. Knowledge gaps: While the research on marine MP is more advanced, there are immense gaps of knowledge regarding freshwater MP. Data on their abundance is fragmentary for large and absent for small surface waters. Likewise, relevant sources and the environmental fate remain to be investigated. Data on the biological effects of MP in freshwater species is completely lacking. The accumulation of other freshwater contaminants on MP is of special interest because ingestion might increase the chemical exposure. Again, data is unavailable on this important issue. Conclusions: MP represent freshwater contaminants of emerging concern. However, to assess the environmental risk associated with MP, comprehensive data on their abundance, fate, sources, and biological effects in freshwater ecosystems are needed. Establishing such data critically depends on a collaborative effort by environmental scientists from diverse disciplines (chemistry, hydrology, ecotoxicology, etc.) and, unsurprisingly, on the allocation of sufficient public funding. Keywords: Chemistry; Ecotoxicology; Environmental quality; Litter; Microplastics; Monitoring; Plastics; Polymers; Review; Water framework directive * Correspondence: wagner@bio.uni-frankfurt.de Department of Aquatic Ecotoxicology, Goethe University Frankfurt am Main, Max-von-Laue-Str. 13, Frankfurt 60438, Germany Full list of author information is available at the end of the article © 2014 Wagner et al.; licensee Springer. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. Wagner et al. Environmental Sciences Europe 2014, 26:12 Page 2 of 9 http://www.enveurope.com/content/26/1/12 Background however, focus almost exclusively on marine plastic debris. Microplastics are freshwater contaminants of emerging However, we argue that microplastics are also freshwater concern contaminants of emerging concern.Thisis supported by Among the multiple human pressures on aquatic ecosys- three arguments. First, although data is scarce, MP are tems, the accumulation of plastic debris is one of the present in freshwater ecosystems. Second, MP contain most obvious but least studied. While plastics generate and adsorb micropollutants and pathogens. Third, labora- remarkable societal benefits [1], there are downsides to tory studies demonstrate that marine organisms ingest our ‘plastic age’. Durability, unsustainable use, and in- MP and suffer adverse effect. While data on freshwater appropriate waste management cause an extensive accu- species is scarce, there is no reason to suppose that they mulation of plastics in natural habitats [2]. In the marine remain unaffected. Thus, concerns about the impact of environment, plastics of various size classes and origins MP on freshwater ecosystems are legitimate and should are ubiquitous and affect numerous species that become receive more scientific attention. entangled in or ingest plastics [3]. Under environmental conditions, larger plastic items State of the science: focus on marine microplastics degrade to so-called microplastics (MP), fragments typ- So far, scientific efforts focus on marine MP, and studies ically smaller than 5 mm in diameter (see Table 1 for on their abundance and effects become increasingly avail- further information). Besides these degradation products able. Because of its high mobility, plastic debris has prac- (secondary MP), MP can also be produced as such (pri- tically permeated the global marine environment [14,15], mary MP). For instance, MP are intentionally used as including the polar regions [2], mid-ocean islands [16], resin pellets (raw material for the production of plastic and the deep sea [17]. Because of their specific hydrol- products) or as ingredient of personal care products ogy, the large oceanic gyres are hot spots of plastic pollu- (e.g., peelings and shower gels). tion (colloquially termed ‘garbage patches’), accumulating MP are of special concern since their bioaccumulation buoyant plastic debris. Here, the plastic abundance often potential increases with decreasing size. MP may be exceeds that of zooplankton [18-21]. With respect to ingested by various organisms ranging from plankton Europe's regional seas, MP have been reported for the and fish to birds and even mammals, and accumulate Baltic, North, and Mediterranean Sea [22-25]. throughout the aquatic food web [4]. In addition, plastics Most of the studies investigate neustonic and pelagic contain a multitude of chemical additives [5] and adsorb MP. However, MP are also present in sediments and have organic contaminants from the surrounding media [6]. been detected on the shorelines and seafloors of six conti- Since these compounds can transfer to organisms upon nents [15,26,27] with typical concentrations ranging from −1 ingestion, MP act as vectors for other organic pollutants 1to 100 items kg [28]. A Belgian study reports a max- −1 [7] and are, therefore, a source of wildlife exposure to imum of 400 items kg in coastal harbor sediments [29]. these chemicals [8,9]. Higher concentrations were reported in a Dutch study −1 Accordingly, MP are considered an emerging global with 770 and 3,300 items kg dry weight sediment in the issue by various experts [10,11] and international institu- Wadden Sea and the Rhine estuary, respectively [30]. Al- tions [12,13]. These concerns and the public interest, though abundant ubiquitously, the spatial distribution of Table 1 Classification of environmental (micro)plastics Category Description Classification Environmental plastics are a very heterogeneous group of litter that can be characterized by various descriptors. In the literature, they are frequently stratified according to size, origin, shape, polymer type, and color. So far, there is no common classification system. Recently, the European MSFD Working Group on Good Environmental Status (WG-GES) provided a ‘Monitoring Guidance for Marine Litter in European Seas’ [76], which represents an important step towards a standardized sampling and monitoring of marine microplastics. Size The WG-GES defines size classes for plastic litter as follows: macroplastics (>25 mm), mesoplastics (5 to 25 mm), large microplastics (1 to 5 mm), and small microplastics (20 μm to 1 mm). Accordingly, items smaller than 20 μm will classify as nanoplastics. Origin Microplastics can also be categorized according to its origin: Primary microplastics are produced as such, for instance as resin pellets (raw materials for plastic products) or as additives for personal care products (e.g., shower gels and peelings). Secondary microplastics are degradation products of larger plastic items, which are broken down by UV radiation and physical abrasion to smaller fragments. Polymers The polymer type of environmental (micro)plastics can be determined by Fourier transformed infrared spectroscopy (FT-IR) or Raman spectroscopy. In concordance to global production rates, high- and low-density polyethylene (HD/LD-PE), polyethylene terephthalate (PET), polypropylene (PP), polystyrene (PS), and polyvinyl chloride (PVC) are the most common polymers found in the environment. In addition, polyamide fibers (nylon) from fishing gears are frequent. Shape The shape can be described according to the main categories: fragments (rounded, angular), pellets (cylinders, disks, spherules), filaments (fibers), and granules [76]. Wagner et al. Environmental Sciences Europe 2014, 26:12 Page 3 of 9 http://www.enveurope.com/content/26/1/12 MP in the marine environment is very heterogeneous Lakes, MP here consisted mainly of low-density poly- [14]. This might be partly due to differences in method- mers (polystyrene (PS), polyethylene (PE), and polypro- ology [28]. pylene (PP)). Field reports on detrimental interactions of plastics Moore et al. [45] provide the first, non-peer-reviewed with biota (e.g., entanglement) are manifold [4]. How- report on MP in rivers. In three Californian rivers, they −3 ever, only about a dozen studies have investigated MP found, on average, 30 to 109 items m . The midstream −3 uptake and effects under laboratory conditions, includ- of the Los Angeles River carried 12,000 items m and −1 ing two studies on freshwater species (literature search will discharge > 1 billion MP items day into the Pacific on ISI Web of Science, search term ‘microplastic*’, man- Ocean. Although very limited, this data indicates that ual filtering). With nine of these papers published since rivers transport relevant amounts of MP. 2012, this is a very recent area of research. The ingestion According to a recent study, the same is true for the of MP by marine invertebrates has been demonstrated in second largest European rivers: Lechner et al. [46] used the laboratory for a broad spectrum of marine species: stationary driftnets and visual inspection to monitor zooplankton [31-33], the lugworm Arenicola marina [34], plastic debris in the Austrian Danube. The authors re- the Blue mussel Mytilus edulis [35-37], and the sandhop- port approximately 900 (2010) and 50 (2012) plastic −3 per Talitrus saltator [38]. M. edulis is the only invertebrate items 1,000 m in the size class of 0.5 to 50 mm. In a in which the transfer of MP from the digestive tract to tis- worst-case scenario, the Danube would discharge 4.2 t −1 −1 sue has been studied and documented [35,36]. plastics day and 1,500 t plastics year to the Black Data on the effects of MP exposure is limited. For zoo- Sea. The latter is more than the total plastic load of the plankton, a reduced algal feeding has been observed [31]. whole North Atlantic Gyre [47]. Lechner et al. provide MP increased the mortality and decreased the fertility in first evidence that large rivers transport significant copepods [32]. In the lugworm, MP reduced the weight amounts of (micro)plastics and thus contribute substan- and feeding and increased the bioaccumulation of plastic- tially to the marine plastics pollution. associated polychlorinated biphenyls (PCBs) [34]. Reduced Because data on the presence of MP in river sediments filtering activity and histological changes as response to is lacking, the Federal Institute of Hydrology and the inflammation have been reported for M. edulis [36,37], al- Goethe University carried out a small, exploratory study though another study did not find significant effects [35]. with sediments from the rivers Elbe, Mosel, Neckar, and In the only study with marine vertebrates, the common Rhine (Germany). Using density separation and visual −1 goby Pomatoschistus microps was exposed to MP and pyr- inspection, we found 34 to 64 MP items kg dry weight, ene [39]. MP delayed the pyrene-induced mortality but in- with the River Rhine containing the highest load. Plastic duced several toxicity biomarkers. In addition, two recent fragments accounted for 60% of the total MP; the remaining studies demonstrate the trophic transfer of MP along the particles were synthetic fibers (Figure 1). Thus, as is the case marine food web from meso- to macrozooplankton [33] for marine and estuarine sediments, river and lake sedi- and from mussels to crabs [40]. ments may be sinks for MP, deserving further investigation. Discussion Sources of microplastics Presence of microplastics in freshwater ecosystems To date, the sources of marine MP are still not very well Despite of the wealth of data on marine MP, to date, characterized. A rough estimation predicts that 70% to only a handful of studies investigate MP in a freshwater 80% of marine litter, most of it plastics, originate from in- context. MP have been detected in the surface waters of land sources and are emitted by rivers to the oceans [12]. the Laurentian Great Lakes [41]. The average abundance Potential sources include wastewater treatment plants −2 in the neuston was 43,000 items km , with a hotspot (WWTPs), beach litter, fishery, cargo shipping, and har- near metropolitan areas, which may represent important bors [12,23,25,29,48]. Although data is so far unavailable, sources. runoff from industrial plastic production sites may be an Three studies report the occurrence of MP in the sedi- additional source. Taken together, most marine studies ments of lakes. Zbyszewski and Corcoran [42] found 0 to tentatively refer to inland waters as relevant sources (in- −2 34 plastic fragments m on the shorelines of Lake Huron deed they are rather transport pathways), while actual data (Canada). Here, MP accumulation may be attributed to is still scarce. the lake's currents and nearby plastic manufacturers. Ex- Inland sources of MP have not been investigated thor- tending their shoreline monitoring to the Lakes Erie and oughly. In analogy to the marine systems, major contrib- −2 St. Clair, Zbyszewski et al. [43] report 0.2 to 8 items m . utors will likely include WWTPs and runoff from urban, Sampling two beaches of Lake Garda (Italy), Imhof et al. agricultural, touristic, and industrial areas, as well as −2 [44] found 100 and 1,100 MP items m at the southern shipping activities. Another potential source is sewage and northern shores, respectively. Similar to the Great sludge that typically contains more MP than effluents Wagner et al. Environmental Sciences Europe 2014, 26:12 Page 4 of 9 http://www.enveurope.com/content/26/1/12 Figure 1 Microplastics in sediments from the rivers Elbe (A), Mosel (B), Neckar (C), and Rhine (D). Note the diverse shapes (filaments, fragments, and spheres) and that not all items are microplastics (e.g., aluminum foil (C) and glass spheres and sand (D), white arrowheads). The white bars represent 1 mm. [49]. Sewage sludge is still frequently used for landfilling Microplastics as vector for other contaminants and as fertilizer in agriculture, and surface runoff may Due to their large surface-to-volume ratio and chemical transfer MP to rivers and lakes and ultimately river ba- composition, MP accumulate waterborne contaminants in- sins and the sea. Washing clothes [26] and personal care cluding metals [53] and persistent, bioaccumulative, and products [50] are sources of MP in WWTPs. Since the re- toxic compounds (PBTs) [54]. A review on the relationship tention capacity of conventional wastewater treatment pro- between plastic debris and PBTs (e.g., PCBs and DDT) has cesses appears to be limited [14], a characterization of MP been published recently [55], and a number of studies exist emission by WWTPs and other sources is urgently needed for polycyclic aromatic hydrocarbons (PAHs) [56-61]. How- to understand where freshwater MP is coming from. ever, there is a lack of information on other important con- taminants like pharmaceuticals and endocrine-disrupting Impact of microplastics on freshwater species compounds (EDCs). Nonylphenol and bisphenol A have In a field report, Sanchez et al. [51] provide the only data been detected in MP [60,62,63]. Fries et al. [24] detected on MP in freshwater fish so far. They investigated various plastic additives in MP, including some well-known gudgeon (Gobio gobio) caught in 11 French streams and EDCs (e.g., phthalates). In addition, Wagner and Oehlmann found MP in the digestive tract of 12% of the fish. Al- [64,65] demonstrated that plastics leach EDCs. Since the though again very preliminary, this field report shows spectrum of contaminants is different in freshwater and that freshwater species ingest MP. However, the rate of marine systems, the chemical burden of freshwater MP re- MP ingestion in different fish species will certainly de- mains to be studied. pend on their feeding strategy. Rosenkranz et al. [52] The interaction of MP and chemicals has been studied demonstrate that the water flea Daphnia magna rapidly in adsorption-desorption experiments [6,57]. While there ingests MP under laboratory conditions. MP (0.02 and 1 is significant complexity in this interaction, MP may act as mm) appear to cross the gut epithelium and accumulate vector transferring environmental contaminants from in lipid storage droplets. This is of specific concern water to biota. While different modeling studies arrive at because MP infiltrating tissues might induce more se- contrasting conclusions [54,66,67], a recent experimental vere effects. Imhof et al. [44] report the uptake of MP by study demonstrates that fish exposed to contaminants annelids (Lumbriculus variegatus), crustaceans (D. magna sorbed to MP bioaccumulate these compounds and suffer and Gammarus pulex), ostracods (Notodromas monacha), adverse effects (glycogen depletion and histopathological and gastropods (Potamopyrgus antipodarum). While the alterations [68]). However, to date, there are too few stud- available studies demonstrate that a broad spectrum of ies investigating whether MP are indeed vectors that facili- aquatic taxa is prone to MP ingestion, the toxicological ef- tate the transfer of organic contaminants to biota. Because fects remain uninvestigated for freshwater species. a verification of the ‘vector hypothesis’ would have major Wagner et al. Environmental Sciences Europe 2014, 26:12 Page 5 of 9 http://www.enveurope.com/content/26/1/12 ecological implications, it deserves further investigation, In a recent ‘Green paper on a European strategy on plas- especially in a freshwater context. tic waste in the environment, ’ the European Commission addresses the issue as part of a wider review of its waste le- Microplastics as vector for exotic species and pathogens gislation [74]. While the Green Paper focuses on potential Not only the complex mix of chemicals contained in and mitigation strategies for plastic litter at the source, it also sorbed to MP and/or ingestion of MP by biota is a cause expresses ‘particular concern’ about MP. for concern but also microorganisms developing biofilms on MP particles. Only very few studies have been con- Conclusions ducted on this issue with marine ecosystems being the Knowledge gaps and research needs focal point of interest [69-72]. Zettler et al. [72] described The investigation of (micro)plastics in aquatic environ- a highly diverse microbial community (‘plastisphere’) ments is a highly dynamic and interdisciplinary area of attaching plastic marine debris in the North Atlantic. Sev- research covering and bringing together the disciplines eral plastisphere members are hydrocarbon-degrading of oceanography and hydrology as well as environmental bacteria which may potentially influence plastic debris monitoring, modeling, chemistry, and toxicology. In recent fragmentation and degradation. But they also found op- years, this collaborative effort advanced our understanding portunistic (human) pathogens like specific members of of the environmental impact of MP, especially by providing the genus Vibrio dominating plastic particles. Therefore, extensive monitoring data. Ongoing research activities MP can act as a vector for waterborne (human) path- focus, however, almost exclusively on marine MP. ogens influencing the hygienic water quality. The fact Data on freshwater ecosystems is at best fragmentary that the microbial communities on MP are distinct from if not absent. This lack of knowledge hampers a science- surrounding water (only some marine bacteria develop based environmental risk assessment of freshwater MP. biofilms on microplastic particles (e.g., [71,72])) suggests Such assessment is needed to facilitate a societal and that MP serve as a kind of new habitat. Until now, the political discussion at national and European levels on the complex interaction between microorganisms/microbial issue, which, depending on the outcome, will result in communities as a key player in aquatic ecosystems/food mitigation measures eventually. For instance, MP could be webs and MP, especially in freshwater, is poorly under- integrated as descriptor of environmental status in the stood and needs to be further investigated. WFD. However, environmental scientists first need to close the gaps of knowledge with regard to exposure and Microplastics in connection to European water policies hazard of freshwater MP and the associated chemicals. The issue of (micro)plastics connects to several European Based on the current state of the science, the following re- water policies. The European Marine Strategy Framework search needs emerge (Figure 2): Directive (MSFD, 2008/56/EC) addresses the issue of marine litter, including plastics. Here, MP are covered by 1. Monitoring the presence of microplastics in Descriptor 10 of Commission Decision 2010/477/EU, freshwater systems. While few studies on large lakes which defines the good environmental status of mar- and rivers are available, we have no clear picture on ine waters [73]. the magnitude of the plastics pollution in surface In contrast, the Water Framework Directive (WFD, 20/ waters. Generating comprehensive monitoring data 60/EC) applying to European inland waters does not spe- on the abundance of freshwater MP is needed to cifically refer to plastic litter. However, the Member States understand their environmental impact. have the obligation to monitor anthropogenic pressures. 2. Investigating the sources and fate of freshwater Here, MP are promising candidates, especially because microplastics. Currently, we still do not understand they might act as vectors for a wide range of freshwater the behavior of MP in aquatic ecosystems. Based on contaminants. For instance, MP have been shown to con- data on their abundance, modeling approaches are tain the WFD priority substances di(ethylhexyl) phthalate needed to identify hotspots and sinks and quantify (DEHP), nonylphenol, octylphenol, and PAHs (2008/105/ loads. One important aspect of understanding the EC, Annex II). environmental fate is also to identify relevant inland Several other European Directives relate to the potential sources of MP and determine the fragmentation sources of freshwater MP, including the Directives on pack- rates of large plastic debris. aging waste (2004/12/EC), waste (2008/98/EC), landfills 3. Assessing the exposure to microplastics. With (1999/31/EC), urban wastewater (91/271/EEC), sewage evidence coming from marine species, it appears sludge (86/278/EEC), and ship-source pollution (2005/35/ plausible that freshwater organisms will ingest MP, EC). In addition, the Union's chemicals legislation (REACH, too. However, actual data is scarce. Environmental 1907/2006/EC) will apply to plastic monomers and addi- toxicologists need to determine the intake of MP by tives of relevant production volumes. freshwater key species. It will be crucial to Wagner et al. Environmental Sciences Europe 2014, 26:12 Page 6 of 9 http://www.enveurope.com/content/26/1/12 Figure 2 Research aspects with regard to freshwater microplastics. All areas need to be investigated more thoroughly to assess the environmental risk associated with microplastics in freshwater ecosystems. understand which plastic characteristics (size, pollutants is very different. Therefore, it is important material, and shape) promote an uptake and what is to investigate the chemical burden of freshwater MP, the fate of MP in the biota (e.g., excretion, including the absorption/desorption kinetics and the accumulation, and infiltration of tissues). These transfer of chemicals from plastics to biota. aspects need to be studied under laboratory 6. Develop a novel framework for the risk assessment conditions and in the field to determine the actual of microplastics. MP can be direct and indirect exposure. stressors for the aquatic environment: They are 4. Evaluating the biological effects of microplastics contaminants of emerging concern per se and, in exposure. Besides abundance and exposure, the addition, may serve as vectors for invasive species and question whether MP induce adverse effects in for other pollutants. To account for that, the classical organisms is crucial to determine their risk assessment framework needs to be adapted. environmental hazard. In the absence of effect For instance, the mixture toxicity of MP-associated studies on freshwater species, one can only speculate compounds and the modulation of the compounds' on potential sensitive endpoints: Ingested plastic bioavailability need to be integrated. fragments may most likely affect the metabolism (starvation due to decreased energy intake) and There are some challenges in investigating these aspects: induce inflammation (when transferring to tissues). To generate commensurable data on the abundance of Because this is an area of research where the least freshwater MP, harmonized monitoring procedures, in- progress has been made so far, the investigation of cluding sampling, identification, and characterization, are MP effects on marine and freshwater species need to needed. For that, the ‘Monitoring Guidance for Marine be intensified considerably. Litter in European Seas’ developed by the European MSFD 5. Understanding the interaction between microplastics Working Group on Good Environmental Status [76] and other freshwater contaminants. Plastics itself can provides an excellent starting point. The separation of contain and release toxic chemicals (e.g., monomers MP from the sample materials (sediments or suspended or plastic additives [75]). In addition, they can particulate matter) and the confirmation of the plastics' accumulate environmental chemicals from the identity to avoid misclassification is still a very resource- surrounding. This may increase the chemical consuming and biased process (e.g., when visually identi- exposure of the ingesting organism and, thus, toxicity. fying MP in complex samples). Here, sample throughput and accuracy need to be increased. Likewise, we need to The findings on chemicals associated with marine MP (mostly POPs) cannot be transferred to freshwaters improve the capability to detect very small MP in the low because here the spectrum and concentrations of micrometer range. Boosting technological innovation in Wagner et al. Environmental Sciences Europe 2014, 26:12 Page 7 of 9 http://www.enveurope.com/content/26/1/12 the area of MP research (e.g., coupling of microscopy and 4. Wright SL, Thompson RC, Galloway TS: The physical impacts of microplastics on marine organisms: a review. Environ Pollut 2013, spectroscopy to identify very small MP) will help meet 178:483–492. those challenges. 5. Dekiff JH, Remy D, Klasmeier J, Fries E: Occurrence and spatial distribution In conclusion, based on our knowledge on the envir- of microplastics in sediments from Norderney. Environ Pollut 2014, 186:248–256. onmental impact of marine MP, their freshwater coun- 6. 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