1 s2.0 S016041202100129X Main

Environment International 152 (2021) 106504
Contents lists available at ScienceDirect
Environment International
journal homepage: www.elsevier.com/locate/envint
Review article
Nano and microplastic interactions with freshwater biota – Current

knowledge, challenges and future solutions
Anna Kukkola a, *, Stefan Krause a, b, c, Iseult Lynch a, c, Gregory H. Sambrook Smith a, Holly Nel a
a
School of Geography, Earth and Environmental Sciences, University of Birmingham, B15 2TT Birmingham, United Kingdom
b
LEHNA- Laboratoire d’ecologie des hydrosystemes naturels et anthropises, University of Lyon, Darwin C & Forel, 3-6 Rue Raphaël Dubois, 69622 Villeurbanne, France
c
Institute of Global Innovation, University of Birmingham, B15 2SA Birmingham, United Kingdom
A R T I C L E I N F O A B S T R A C T
Handling Editor: Frederic Coulon Current understanding of nano- and microplastic movement, propagation and potential effects on biota in
freshwater environments is developing rapidly. Still, there are significant disconnects in the integration of
knowledge derived from laboratory and field studies. This review synthesises the current understanding of nano-
and microplastic impacts on freshwater biota from field studies and combines it with the more mechanistic
insights derived from laboratory studies. Several discrepancies between the field and laboratory studies,
impacting progress in process understanding, were identified including that the most prevalent plastic mor
phologies found in the field (fibres) are not those used in most of the laboratory studies (particles). Solutions to
overcome these disparities are proposed to aid comparability of future studies. For example, environmental
sampling and separation of biota into its constituents is encouraged when conducting field studies to map
microplastic uptake preferences. In laboratory studies, recommendations include performing toxicity studies to
systematically test possible factors affecting toxicity of nano- and microplastics, including morphology, chemical
makeup (e.g., additives) and effects of plastic size. Consideration should be given to environmentally relevant
exposure factors in laboratory studies, such as realistic exposure medium and effects of plastic ageing.
Furthermore, based on this comprehensive review recommendations of principal toxicity endpoints for each of
the main trophic levels (microbes, primary producers, primary consumers and secondary consumers) that should
be reported to make toxicity studies more comparable in the future are given.
1. Introduction To date, a vast majority of plastic research has focused on marine and
coastal environments (Desforges et al., 2014; Kanhai et al., 2017; Lusher
Plastic pollution in the world’s oceans is a widely reported issue et al., 2015; Munari et al., 2017; Van Cauwenberghe et al., 2015;
(Cózar et al., 2014; Geyer et al., 2017; Jambeck et al., 2015). Besides the Woodall et al., 2014) with the transport, fate and impact of plastics in
visible macroplastic, there is also concern surrounding smaller plastics, freshwater systems only recently gaining attention (Li et al., 2018;
such as microplastics (dimension less than 5 mm) (Arthur et al., 2009; Krause et al., 2021). This is likely driven by the increasing realisation
GESAMP, 2016; Thompson et al., 2004), and nanoplastics (despite some that lakes and rivers are not merely conduits transporting MnP from
ongoing debate in the literature generally considered less than 1000 terrestrial sources to the marine environment, but also have the poten
nm). These micro and nanoscale plastics are referred to hereafter as tial to act as temporary/long-term sinks (Hurley et al., 2018; Luo et al.,
MnP, unless specifically only micro or nanoplastics are discussed. MnP 2019b). There is, thus, a risk that MnP may cause detrimental effects to
can be either directly designed and produced for this specific size-range freshwater ecosystems.
(primary), or result from breakdown of macroscale plastic into smaller Microplastics have been found in the surface waters and sediments of
pieces (secondary) due to physical, photochemical and/or biological both rivers and lakes (Eerkes-Medrano et al., 2015; Li et al., 2018;
degradation (Corcoran et al., 2009; Dawson et al., 2018; Mateos- Tibbetts et al., 2018). They can enter freshwater systems via various
Cárdenas et al., 2020; O’Brine and Thompson, 2010; Zbyszewski et al., pathways, such as outfall from waste water treatment plants (WWTP)
2014). (Murphy et al., 2016), or through surface runoff (Corradini et al., 2019;
* Corresponding author.
E-mail address: [email protected] (A. Kukkola).
https://doi.org/10.1016/j.envint.2021.106504
Received 24 November 2020; Received in revised form 1 March 2021; Accepted 2 March 2021
Available online 15 March 2021
0160-4120/© 2021 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
A. Kukkola et al. Environment International 152 (2021) 106504
Kole et al., 2017; Liu et al., 2019a). Microplastics can also find their way 1. Identify freshwater species shown to be capable of interacting with
into freshwater systems through transport via air and accumulate as dry MnP in the field and the laboratory at the different trophic levels;
or wet deposits (Allen et al., 2019; Dris et al., 2017, 2016). Although the 2. Establish potential patterns in the freshwater MnP literature
extent of our knowledge is not the same for nanoplastics, due to including types of plastics found/used, geographical context and the
extraction (sampling) and detection limitations, it is suspected that physical characteristics of the MnP assessed;
nanoplastics are present everywhere that microplastics are, and may 3. Identify key areas for increased alignment of laboratory and field
follow similar transport and fate pathways to those of microplastics research, to facilitate risk assessment, and the priority challenges for
(Wang et al., 2021). future research, for which we propose solutions.
MnP interaction and/or ingestion and their effects have been docu
mented for a variety of freshwater biota, such as algae, zooplankton, fish 2. Methods
and birds (Faure et al., 2015; Sadler et al., 2019; Wu et al., 2019)
(Fig. 1). A comprehensive literature review was carried out using Web of
There is some initial evidence of pollutant transfer from MnP to or Science with the following topic search equation:
ganisms (Coffin et al., 2019; Rochman et al., 2013; Wardrop et al., TS=(((microplastic* OR nanoplastic*) AND (freshwater OR lake OR
2016). However, it is still debated whether MnP can be considered an river)) AND (ingestion OR abundance OR occurrence OR content OR
environmentally relevant pathway for sorbed pollutants (Hartmann quantity OR feeding OR contamination OR gut OR intestines OR gastroin
et al., 2017; Koelmans, 2015; Koelmans et al., 2016). Nevertheless, MnP testinal OR bioaccumulation OR bioavailability OR uptake OR organism*))
could be toxic to biota in their own right through physical effects, such Publications for the period 2011 and 2020 have been included in this
as slowed egestion times (Au et al., 2015; Shang et al., 2020), that could review. Studies were analysed using the following four criteria: 1)
lead to clogging or damage of intestinal tracts (Lei et al., 2018). This, Original study (reviews were excluded), 2) Focus on freshwater eco
together with the realisation that MnPs are omnipresent in freshwater systems (salinity less than 0.05% or 0.5 ppt), 3) Report results showing
systems, has led to an expansion of interaction and toxicity studies in an interaction between MnP and freshwater organisms, and 4) Quan
freshwater organisms. However, this research field is still in its infancy tifies or uses plastics less than 5 mm in diameter (Arthur et al., 2009;
and potential entry points, uptake mechanisms, and fate for MnP in biota GESAMP, 2016; Thompson et al., 2004). The initial search yielded 878
and consequently into food-webs have not yet been clearly established matches from which 656 articles were excluded due to not conforming
(Krause et al., 2021; Wong et al., 2020). In particular, analytical with the criteria set above. An additional 18 articles met the criteria for
methods to quantify MnP burden are still being optimised for environ inclusion after citation analysis was carried out for the studies included
mental matrices (O’Connor et al., 2020) and biological tissues (Wagner from the first step, bringing the total number of journal articles reviewed
et al., 2017). There are also questions regarding how well laboratory for this synthesis to 240 (Table S1).
studies reflect field data and vice versa. This review aims to provide a The studies were divided into field or laboratory based research.
pathway forward whereby harmonisation between field and laboratory Studies were also grouped into: algae, vascular plants, microbes, cla
studies is discussed. This extensive review of over 76 field and 164 docerans (separated from the rest of crustaceans, due to high occurrence
laboratory studies also aims to find commonalities amongst published in the literature), crustaceans, gastropods, dipterans, bivalves, annelids,
literature that may support future studies by providing a solid baseline amphibians, fish, birds, and others. These biota groups were then
against which to design and implement future experimental and sam organised into the following four trophic levels:
pling campaigns, thereby maximising their increased comparability and 1. Microbes
utility for risk assessment. Therefore, a comprehensive synthesis of 2. Primary producers (algae, vascular plants)
current research on MnP interactions with freshwater biota was per 3. Primary consumers (cladocerans, crustaceans, gastropods, dip
formed to: terans, bivalves, annelids and others)
4. Secondary consumers (amphibians, fish, and birds).
Fig. 1. Conceptual model for MnP movements in the

freshwater food web. Numbers (1–16) indicate that
MnP interaction with this biotic group has been
confirmed (Table S1). Species in the figure: 1) Anas
platyrhynchos, 2) Cygnus olor, 3) Lemna minor, 4)
Fulica atra, 5) Lepomis macrochirus, 6) Chlorella vul
garis, 7) Daphnia magna, 8) Esox lucius, 9) Gobio gobio,
10) Squalius cephalus, 11) Microhyla ornate, 12)
Alburnus alburnus, 13) Dreissena polymorpha, 14) Tu
bifex tubifex, 15) Gammarus pulex and 16) Chironomus
spp.
2
From each of these trophic levels the following were identified; 1) frequently used plastic was PS, followed by PE, ‘others’, PP and PET.
species studied, 2) physical (i.e., size, morphology, colour) and chemical Here also, several papers used a commercial microplastic for which no
(i.e., plastic type) characteristics of the MnP identified (field) or used compositional information was available (grouped as “others”),
(laboratory) and 3) methodologies (characterisation and toxicity end reducing the utility of the data for risk assessment.
points) used. Toxic effects were included in the context of identifying
potential endpoints that could be used for baseline studies, but were not
extensively reviewed, as this topic has been covered previously (e.g., 3.3. Sizes and morphology of plastics
Anbumani and Kakkar, 2018; Prokić et al., 2019; Triebskorn et al.,
2019) and was considered to be out of the scope of this study. Most of the studies fell into the size range of microplastics, with re
Size was divided into two separate categories; microplastics (1–5000 ports on nanoplastics being absent from field studies. Twenty-six percent
µm) and nanoplastics (<1000 nm). Morphology of plastics was assigned of field studies did not report the respective size of the observed plastics
into three main categories; a) fibres, b) particles (that encapsulated both (Fig. 3), while laboratory studies included size by stating the commercial
spheres and granules due to lack of morphology characterisation in size range and in some instances provided additional size characteriza
several studies) and c) fragments. tion information, via techniques such as dynamic light scattering (DLS)
To identify any regional hotspots of MnP research, the origin of and/or scanning electron microscopy (SEM).
laboratory studies was assessed according to the locations of the first and The most prevalent morphology reported in field studies, where this
last author’s facilities/addresses, while field studies had their respective information was available, was fibres (76.5%). However, particles were
sampling location(s) recorded independently of the author’s respective the most abundant morphology used (76.2%) in laboratory settings,
locations. with fibres used in eight studies (4.8%).
3. Results
3.4. Geographical spread
3.1. General results
Analysis of the spatial distribution identified some clear geograph
From the 240 studies, 76 (~32%) field studies and 164 (~68%) ical hotspots for MnP research. The majority of laboratory studies
laboratory studies were identified (Table S1). originated from China (n = 43), North America (n = 20) and Europe
(Germany (n = 22), Italy (n = 11) and UK (n = 11)) as shown in Fig. 4.
This spread in laboratory studies is matched by patterns identified in the
3.2. Types of plastics sampling locations of field studies, that were clustered in Europe (n =
22), North America (n = 14) and China (n = 15).
Polyethylene (PE) was the most common plastic type found in field
studies, followed by polypropylene (PP), polyethylene terephthalate
(PET), polyamide (PA) and polystyrene (PS), as shown in Fig. 2. ‘Not 3.5. Trophic levels and biota groups
given’ was the largest group in field studies, highlighting the lack of
chemical verification tools used, with forty-two percent of studies not From the four trophic levels including thirteen biota groups defined
including polymer identification. In laboratory studies, the most above, fish were the most studied (n = 90) making up ~59% of field
studies and ~27% of laboratory studies. This was followed by cladoc
erans (n = 43), which were all laboratory studies (Fig. 5).
Fig. 3. Relative abundance of studies per MnP size class. Note that studies that
Fig. 2. Most common MnP plastic types reported across laboratory and included MnP from different size classes were counted as separate studies for
field studies. the purpose of this figure.
3
Fig. 4. Number of laboratory studies per country, grouped via first and last authors of the studies and locations of the field sampling sites.
studies, it is recommended to extend laboratory effect testing to a more

diverse range of plastic types. Special consideration should be given to
those identified in biota from field studies, such as PA and cellophane, as
the current trend favours certain plastic types and makes results difficult
to compare
Regional hotspots for laboratory and field research were found to
largely overlap (Fig. 4). Critically, Asian (apart from China) and African
systems appear under-represented despite many of these regions, such as
South and Southeast Asia, having been identified as being amongst the
most plastic polluted areas globally (Jambeck et al., 2015; Lebreton
et al., 2017). The identified lack of field studies in these areas is there
fore of concern, as this impedes our holistic understanding regarding
global MnP pollution and its impacts on biota. Furthermore, the total
number of field studies is still relatively low (n = 76), when compared to
laboratory studies. More observations are thus required, especially in
highly polluted and under-represented regions, such as parts of South
east Asia and Africa (Nel et al., 2021b).
There was a clear predisposition towards laboratory studies in all
biotic groups, with the exception of fish and birds (Fig. 5). Studying
higher trophic level organisms in laboratory settings can pose ethical
challenges, as well as being time consuming, which can partly explain
this trend. From all biotic groups, fish were the most studied. Fish
represent one of the largest classes of Animalia in freshwater systems
Fig. 5. Number of published MnP interaction studies in freshwater biota and can stretch over several trophic levels and feeding guilds. As they
groups. Note that one field study and some laboratory studies included more are generally higher up in the food chain and have commercial impor
than one biota group and each species is counted separately for this figure. tance and health implications for humans via consumption, it is logical
that studies on MnP ingestion have focused on this group. However,
4. Discussion more studies are required across the different biotic groups to map out
the occurrence of MnPs in the field and to identify their potential
4.1. General discussion ecosystem-level effects. In addition to more field studies, we identified
three key challenges that freshwater MnP research is currently facing,
The major plastic types used in laboratory settings and found in biota described below, along with proposed solutions to overcome them,
loosely follow the trends in global plastic production. According to which have also been summarised into Tables 1 and 2.
PlasticsEurope (2020), the major plastics manufactured in 2019 were PE
(29.8%), PP (19.4%), polyvinyl chloride (PVC) (10%), polyurethane
4.2. Challenges for future research
(PUR) (7.9%), PET (7.9%) and PS (6.2%). A similar trend was observed
in field studies (Fig. 2), with PE and PP being the most common plastic
4.2.1. Challenge 1: The mismatch between field and laboratory studies
types identified from the field samples, while the most common plastics
In order to predict effects of MnP on biota and freshwater ecosys
used in laboratory studies were PS, followed by PE, PP and PET.
tems, exposure scenarios used in the laboratory should reflect real
Although most common plastic types are well represented in laboratory
environmental conditions as closely as possible. Here, we explore the
4
Table 1 biota (Akindele et al., 2019; Li et al., 2020a; Lv et al., 2019; Nel et al.,
Recommendations for field sampling that aims to understand the interplay be 2018; Su et al., 2018, 2016; Yan et al., 2019). For example, Lv et al.
tween ingested MnP and environment. (2019) found that the microplastic composition was similar between the
Recommendations crayfish Procambarus clarkii and surrounding sediments, with fibres
Collection of field samples Sediment and water samples (background
prevalent in both. Furthermore, Su et al. (2018) found that the micro
inconjunction with biota samples concentrations needed for assessment of plastic load in bivalves at the Yangtze River basin was significantly
potential biomagnification) dependent on both water and sediment microplastic contamination. In
Separation of organism into Stomach, muscle, liver and brain when contrast, Su et al. (2016) reported that the microplastic load in bivalves
itsconstituents applicable (i.e. fish) and quantification of MnP
was negatively correlated with the contamination in surrounding sedi
load in each
Usage of relevant digestion method KOH, NaOH or similar. Match to that used for ments. However, with only a handful of studies collecting data on MnP
environmental samples contamination from all compartments, this relationship remains
Identification methods Tagging methods, such as fluorescent dyes, inconclusive.
Chemical identification, such as FT-IR, Raman The prevalence of fibres could also be an indication of preferential
spectroscopy or GC-MS (50% of putative MnP)
Recording physical characteristics of Colour (where possible), morphology and size
consumption by certain biotic groups, especially in fish (Collard et al.,
MnP 2019). There is evidence from laboratory studies that visually orientated
Reporting Lowest detection limit and internalised dose, as fish actively forage on MnP resembling their prey items (Roch et al.,
follows; number mg− 1 tissue, mg mg− 1 tissue 2020). Indeed, Yuan et al. (2019) noted that the proportion of white
and items individual− 1
fibres in goldfish from Poyang Lake, China, was higher than that found
Method development To enable nanoplastic identification from the
field samples in the surrounding environment, which could indicate confusion with
prey species, such as mosquito larvae or zooplankton. This is further
supported by McNeish et al. (2018) where microplastic colours varied in
surface water collected within the tributaries of Lake Michigan, (USA),
Table 2
Recommendations for laboratory studies that aim to systematically understand
which was not reflected in the fish who preferentially ingested blue and
the drivers and toxicological effects of MnP exposure. transparent fibres. Hurley et al. (2017) reported an absence of
microbeads in the freshwater worm Tubifex tubifex, even though they
Recommendations
were found in the surrounding sediment. Similarly, Schessl et al. (2019)
Morphology Carry out exposures with similar parent plastic but different reported an absence of microbeads in bivalves Dreissena polymorpha and
morphology (i.e. fragments, fibres and spheres)
D. bugensis despite their presence in the environment. Drivers of this
Chemical 1) Identify chemical fingerprint: e.g., colourants, plasticisers
composition 2) Wash a sub-set of parent plastic for toxicity assessment of apparent preferential uptake remain unknown; possibilities include size,
leachates 3) Avoid usage of proprietary polymers whose morphology, biofouling and/or plastic type. Laboratory studies have
composition is unknown begun focusing on this question, with Li et al. (2019) stating that uptake
Size 1) Systematic testing of similar parent plastic in different sizes of plastic fibres in bivalves was related to the elastic modulus, i.e.,
e.g., PS 1 µm, 5 µm and 10 µm, match exposure dose by surface
area, mass and MnP number
“softness” of the plastic type. It is essential to test these possible drivers
Exposure 1) Environmental considerations in laboratory settings.
i.e., always provide food, consider the presence of organic An alternative explanation may be that fibres are accumulating in the
matter, natural medium and mode of exposure etc. gastrointestinal (GI) tracts of biota due to their elongated shape. There is
2) Aging of the plastic
some initial support for this hypothesis; the only two field studies that
i.e., Pristine vs aged (natural or laboratory aged)
3) Abundance separated the individual fish into different parts (i.e., stomach, muscle,
i.e., Inclusion of lower concentrations with life-time exposure gills and liver), reported different microplastic morphologies present in
the various regions. For example, Collard et al. (2018) indicated that in
3) Duration field conditions PS and PE fragments ranging from 147 to 567 μm
i.e., Extended monitoring periods and consider depuration
steps
appeared to translocate into the livers of European chubs Squalius
Endpoints 1) Microbes cephalus after ingestion, while fibres were prevalent in the stomach.
Similarly, Garcia et al. (2020) reported microplastic films being more
i) Principal endpoints: taxon richness prevalent in gut tissues of Prochilodus magdalenae and Pimelodus gros
ii) secondary endpoints: species specific preference for plastic
skopfii whereas fragments were more prevalent in muscle and gills.
type
2) Primary producers Microfibre retention in the gut was also observed by Au et al. (2015) in a
i) Principal endpoints: photosynthetic activity and growth laboratory study, where PP fibres remained in the gut of the crustacean
ii) Secondary endpoints: gene regulations and stress responses Hyalella azteca for longer than natural food and/or PE particles. This
3) Primary consumers offers some initial support for the hypothesis that fibres could be
i) Principal endpoints: growth and mortality
ii) Secondary endpoints: reproduction and multigenerational
retained in the gut for a longer duration. However, more research is
studies needed targeting gut retention times of fibres.
The apparent dominance of fibres in field samples could also be a
4) Secondary consumers result of overestimation due to methodological bias in the applied
i) Principal endpoints: growth, mortality and reproduction
analytical approach. For example, 31 out of 69 field studies (excluding
ii) Secondary endpoints: behavioural changes, AChE and
oxidative stress studies on microbes) did not use any chemical verification tools and
relied solely on visual identification and/or a hot needle test to confirm
the presence of plastics. It is plausible that during the visual identifi
mismatch between field and laboratory studies and suggest solutions to cation, the larger, less ambiguous fibres are more readily identified
close this gap. compared to other morphologies. The lack of chemical verification
Fibres were the most prominent microplastic morphology identified means that the identified fibres could also be natural or cotton fibres.
across taxa in field studies. This trend potentially reflects the relative Moreover, only six of the analysed papers stated clearly the lower size
abundance of fibres in the environment, as fibres are commonly iden detection limit (Domogalla-Urbansky et al., 2019; Park et al., 2020;
tified in freshwater studies (e.g., Dris et al., 2015; Luo et al., 2019b; Roch et al., 2019; Winkler et al., 2020; Xiong et al., 2018; Yuan et al.,
Wang et al., 2017). There appears to be a relationship between micro 2019). This raises questions about the ‘non-detected’ fraction, and un
plastic load within sediment and water, and microplastic burden within derestimation of smaller plastics could lead to overestimation of the
5
pervasiveness of more easily identified fibres. confound results, especially if information about chemical composition
In order for the research community to address these challenges, and additive content is not given. However, all fibres studied to date,
there is a need to improve the extraction of MnP from field biotic sam regardless of the source, have shown negative effects on biota. It is clear,
ples: Firstly, relying on visual identification solely should be minimised, however, that there are not enough studies focusing on the effects of
as this can discriminate against smaller MnP which are more difficult to fibres and their leachates to build a full picture of their deleterious ef
identify. The use of tagging methods, such as fluorescent dyes, for fects, and more systematic testing of different plastic fibre types (such as
example, Nile Red (Erni-Cassola et al., 2017; Maes et al., 2017; Nel et al., PET fibres in different lengths and colours) on multiple biota groups in
2021a; Shim et al., 2016) that can reduce visual bias, should be explored needed.
(Table 1). Researchers are encouraged to refer to the reporting guideline The respective size classes found/used in field and laboratory studies
checklist and quality criteria published by Cowger et al. (2020), Collard also differed (Fig. 3). The absence of nanoplastics in field data can be
et al. (2019) and Hermsen et al. (2018). Secondly, the lower detection attributed to the current challenges in sample collection, extraction and
limit (where putative MnP can be confidently identified) should always quantification methods (Nguyen et al., 2019; Schwaferts et al., 2019).
be reported in order to facilitate comparability between studies These smaller plastics should, however, be the focus of future research,
(Table 1). as it is predicted that smaller plastics are more numeric, both in the
Thirdly, where applicable (e.g., fish), it is important to separate the environment and in biota (Roch et al., 2019; Triebskorn et al., 2019).
biota samples into different parts, such as brain, muscle, liver and gut
(Table 1), which can give more specific information on where MnP are 4.2.2. Challenge 2: Baseline studies comparing physical and chemical
found and any preferential distributions (Collard et al., 2018; Garcia characteristics of MnPs and their effects on toxicity
et al., 2020). More studies including this step are required, as there is To fully understand and map the effects of different MnP, a shift
contrasting evidence on tissue translocation (Collard et al., 2017; Eliz towards systematic reporting of MnP morphology, chemical makeup and
alde-Velázquez et al., 2020; Jovanović et al., 2018; Zeytin et al., 2020; size under specific exposure conditions is needed to allow correlation of
Zitouni et al., 2020) and disagreement exists particularly regarding the properties with potential toxic effects. Here, we introduce four major
size fractions that are capable of translocating into tissues (as reviewed factors that could affect the MnP toxicity, each of which needs to be
by Triebskorn et al. 2019). In the field of nanomedicine, it is generally separately and systematically tested. Special attention should be given
accepted that endocytosis pathways are limited to particle sizes up to 5 to realistic environmental exposure scenarios in terms of exposure me
µm (Kou et al., 2013; Zhang et al., 2009), raising questions regarding any dium and the presence/absence of natural compounds, as well as the
potential mechanisms for translocation of larger items. It is plausible impact of aging of the MnP compared to effects of pristine MnP.
that bigger fragments (>20 µm) could be methodological artefacts or i. Morphology
contamination from processing of the samples, if not enough rigor is Plastic fibres have been reported to be more harmful than other
applied. However, granuloma formation has been proposed as a po tested morphologies (i.e., particles). For example, Au et al. (2015) re
tential entry pathway for MnP into muscle tissue (Zeytin et al., 2020). ported that acute exposure to PP fibres (20–75 μm at 45 fibres mL− 1)
Digestion should be carried out for each separate body part, with the reduced the growth rate of crustacean H. azteca in a dose dependent
same digestive method, such as KOH (Karami et al., 2017a; Thiele et al., manner whereas exposure to PE particles (10–27 μm at 1 × 105 particles
2019), followed by the extraction step and chemical analysis (such as mL− 1) did not. In this case it is difficult to determine whether the
ZnCl2 separation followed by Fourier-transform infrared (FT-IR) or morphology or the chemical characteristics were causing the deleterious
Raman spectroscopy), and where possible 50% of putative MnP should effect of PP as no controls with similar morphologies were carried out.
be analysed (Hermsen et al., 2018) (Table 1). Extra care should be taken Ziajahromi et al. (2017) reported a lower LC50 (lethal concentration
to reduce any false-positives, such as dislocation or introduction of required to kill 50% of test population) value in Ceriodaphnia dubia for
particles and/or fragments during dissection and rigorous control PET fibres (280 ± 50 μm at 5 × 10− 4 mg mL− 1 or 13 fibres mL− 1) than
measures should be in place. for PE particles (1–4 μm at 1 × 10− 3 or 74 particles mL− 1). This, how
Fourthly, to fully address the possibility of the selective uptake of ever, does not translate directly into fibrous MnP being more delete
MnPs and to examine which factors in the immediate environment drive rious, as morphology along with any additives and plasticisers, total
their ingestion, environmental samples (water column and sediment) surface area and particle number differences may have confounded
should always be collected and analysed to characterise the sizes, these results. It is also plausible that mode of exposure, i.e., how biota
morphologies, colours and types of MnPs present (Table 1). The diges are exposed to MnP, could affect their harmfulness. For example,
tion, extraction and chemical analysis methods used for the environ exposure of C. dubia to PET fibres resulted in more severe effects on body
mental samples should match as closely as possible to those used for size and neonate numbers than exposure to PE particles despite having
biota, in order to reduce any methodological bias. This would inform on no fibres in their guts (Ziajahromi et al., 2017), suggesting that fibres
the possible drivers of fibre uptake and would aid in the prioritisation of caused physical harm but not via ingestion. Thus, the mode of exposure
plastics for laboratory exposure experiments. can play an important role in determining the effects of MnPs and should
Despite fibres being the most common morphology reported in the be taken into consideration in the study design (see iv. Environmental
field, this is not reflected in laboratory studies, which most commonly factors).
employed particles. Only 8 out of 164 laboratory studies used fibres in In order to fully address to what degree the plastic morphology may
MnP interaction studies (Table S1), and only six studied their effects, impact toxicity, tests using the same/similar parent plastic with different
from which all reported negative effects on the test species. For example, morphologies must be carried out (Table 2), and the observed effects
decreased growth was seen in the crustacean H. azteca and planarian must be differentiated by physical versus chemical damage where
Dugesia japonica exposed to 20–75 μm PP fibres (Au et al., 2015) and possible (direct and indirect effects). Use of computational image de
~30 μm PET fibres (Gambino et al., 2020) and the freshwater flea scriptors for shape, such as circulatory, convexity and main elongation,
Daphnia magna showed increased mortality rates when exposed to which can be determined with transmission electron microscopy (Var
60–1400 μm PET fibres (Jemec et al., 2016). sou et al., 2020), may provide an useful approach to normalise between
The type and origin of fibres used in these studies also varied. For different morphologies and enable direct comparison of non-spherical
example, Au et al. (2015) used aged PP marine rope. Jemec et al. (2016) morphologies.
used milled PET fabrics and Gambino et al. (2020) produced PET fibres ii. Chemical composition
in their laboratory. Evidence suggests that additives may influence MnPs found in nature consist of a complex mixture of monomers,
toxicity (Boyle et al., 2020; Capolupo et al., 2020), therefore the same plasticisers, colourants and other additives (OECD, 2014a). Therefore,
plastic type from different commercial sources/products may further to fully understand the effects of MnP, it is not sufficient to report and
6
identify the different parent plastic types only (Fig. 2), but also their to Diptera C. tepperi in synthetic water but not in river water, indicating
chemical make-up, including additives, such as plasticisers, flame- that consideration should be given to more realistic exposure media and
retardants and colourants should be documented. Different MnP leach their effects on toxicity. As discussed previously, mode of exposure
ates have shown different degrees of effect on the freshwater algae might also play a key role; for example C. tepperi exposed to PE in
Raphidocelis subcapitata (Capolupo et al., 2020), while the leachate from sediment (500 particles Kg− 1) showed increased mortality (Ziajahromi
PVC was more toxic to zebrafish Danio rerio larvae than the plastic et al., 2018), while exposure in water (1600 particles L− 1) showed no
fragments themselves (Boyle et al., 2020). Similar leaching of additives effect (Ziajahromi et al., 2019 Table S1), indicating that how biota is
(such as Bisphenol A) has been demonstrated in simulated gut condi exposed needs to be accounted for when planning experiments, and
tions of marine biota (Coffin et al., 2019). As this leaching of additives consideration should be given to whether this reflects environmentally
could affect the observed toxicity, there is a need to differentiate be realistic modes of exposure.
tween the toxicity of parent plastic and any specific additives. For It is also important to understand how laboratory exposure concen
example, routine washing of a sub-set of the parent plastic should be trations compare with those observed in the environment. However, this
carried out to remove leachable additives, followed by parallel testing of can be problematic, as reported units for laboratory and field studies
the pristine and washed MnP and the leachate (Table 2), as this may varied. Exposure concentrations in laboratory studies were often mass
shed important light into the exact drivers of any observed toxicity. per volume (mg L− 1) but reporting also MnP number and surface area
The use of commercial polymers, where the composition is unknown might be more informative. Conversely, field studies reported mg indi
should be discouraged in toxicity testing, and complete chemical map vidual− 1, or more often item individual− 1, making it difficult to compare
ping should be carried out for plastics used in the experiments. If this is the results between the two. In laboratory studies, it is common to use
not possible, the composition should be identified as a minimum to the concentrations that span the expected effect threshold to ensure that an
level of parent polymer/copolymer. Typical equipment used to identify effect will be observed. Indeed, it is not uncommon to see arguably
parent plastic type includes FT-IR, Raman spectroscopy or similar. unrealistic exposure concentrations (e.g., De Felice et al., 2019; Li et al.,
Identification of the additives could be carried out using equipment like 2020c) in laboratory studies. It is difficult, however, to predict what can
gas chromatography–mass spectrometry (GC-MS), which would also be be considered as ‘environmentally relevant’ concentrations, as there is
useful to extend emerging databases on plastic additives and spectra uncertainty regarding the abundance of smaller MnP in the environment
(Rochman, 2020) and to correlate specific plastic sources with specific and occurrence of bigger microplastics varies with location (Li et al.,
combination of additives that may prove diagnostic. 2018). Furthermore, the units used to report environmental concentra
iii. MnP size tions are often item m− 3 (water) and item Kg− 1 (sediment), making it
It has been shown in marine settings that plastic size can play an hard to relate directly to laboratory exposures which tend to report units
important role in MnP toxicity (Jeong et al., 2016; Lee et al., 2013). as mass volume− 1. Regardless, it is imperative for the scientific com
Similar size-dependant effects have been observed in freshwater species, munity to expand the toxicity testing into lower exposure doses (such as
for example, Lei et al. (2018) found that mortality of nematodes was MnP concentrations of 100 items L− 1) (Triebskorn et al., 2019) with
related to the size of PS MnP (1.0 μm were less lethal than 0.1 or 5.0 μm). extended exposure time scales to cover life-time and/or multiple gen
Similarly, the effect of PE MnP in dipterans Chironomus riparius and erations (Table 2). For example, Kelpsiene et al. (2020) showed that
C. tepperi was more pronounced with decreasing particle sizes (Silva when D. magna was exposed to 0.32 mg L− 1 of 26 or 62 nm PS over its
et al., 2019; Ziajahromi et al., 2018). full life-time, increased mortality became obvious, which was not pre
It has also been observed that nanoplastics had a higher toxicity than viously reported in acute 24 h exposures to 400 mg L− 1 (Mattsson et al.,
microplastics in the freshwater flea D. magna (Ma et al., 2016). This 2017).
higher toxicity could be related to nanoplastics ability to cross cell-walls
and accumulate in sites such as the egg-yolk sacs of water flea, the gills, 4.2.3. Challenge 3: Harmonisation of endpoints reported for each trophic
gut and liver of zebrafish, and the digestive gland of the bivalve Elliptio level
complanata (Auclair et al., 2020; Brandts et al., 2020; Chae et al., 2018; To facilitate inter-comparability of MnP toxicity data, common
Lu et al., 2016; Parenti et al., 2019). Indeed, size dependent toxicity principal endpoints need to be identified for each trophic level, which
needs to be systematically tested using similar parent plastic type should be included in each study as minimum. Here, potential principal
(Table 2). endpoints for the four trophic levels identified in this paper (Fig. 6,
iv. Environmental exposure considerations Table 2) are introduced, including justification for why these endpoints
To fully address the drivers behind MnP toxicity, all potential should be included in future studies.
contributing factors i.e., morphology, composition and size, need to be i. Microbes
addressed in a proper environmentally relevant context (Table 2). Here, For microbes, the taxon richness and its possible changes when in
much can be learned from the nanomaterials eco-toxicological field, contact with different plastic types is the most important reporting
where formation of an eco-corona, biofouling and ageing of the mate requirement. There is evidence that MnP can act as a favourable sub
rials are increasingly recognised as being essential to realistic exposure strate for specific microbial communities (Hoellein et al., 2017; Kettner
and hazard assessment studies (Ellis et al., 2020; Nasser et al., 2020). It et al., 2019; Li et al., 2020b; McCormick et al., 2014, 2016). For
is important to realise that aging of plastics and other mechanisms such example, McCormick et al. (2014), McCormick et al. (2016) and Kettner
as adsoprtion of organic matter may affect the physical properties of the et al. (2019) found a lower species richness on microplastic surfaces
plastics. For example, growth inhibition of freshwater algae Scenedemus when compared to the surrounding environment. This is further sup
subspicatus and Chlamydomonas reinhardtii were found to be greater ported by Parrish & Fahrenfeld (2019) and by Kelly et al. (2020) who
when exposed to aged or weathered rather than pristine plastics (Bau demonstrated that PE and PS particles (125–500 μm) and fragments
drimont et al., 2020; Wang et al., 2020b). Furthermore, Liu et al. (0.25–0.5 mm) exhibited distinct microbial communities irrespective of
(2019b) found that when zebrafish were co-exposed to1 μg L− 1 and 1 mg the source water. Common human pathogens, such as arcobacters (Gong
L− 1 of nano-sized PS (50–100 nm) and fulvic and humic acid, the et al., 2019; Kettner et al., 2019; McCormick et al., 2014, 2016)
reactive oxygen species (ROS) levels were stimulated synergistically. In frequently colonise plastics, and certain antibiotic resistant genes can be
contrast, the presence of these natural acidic organic polymers reduced aligned with the presence of microplastics (Ram and Kumar, 2020;
the ROS level in freshwater algae Scenedesmus obliquus, suggesting that Wang et al., 2020a), thus the likelihood of MnP acting as a transport
the presence of natural compounds in the medium affects MnP toxicity medium cannot be negated. Hoellein et al. (2017) suggested that this
(Liu et al., 2019b). Furthermore, Ziajahromi et al. (2018) reported that preference was enhanced closer to a WWTP and diluted further down
PE particles (10–27 μm) reduced the toxicity of the insecticide bifenthrin stream. Studying taxon richness and specifying any potential
7
Fig. 6. Potential principal and secondary toxicity endpoints for the four trophic levels.
preferential colonisation needs to be tested with different plastic types in inhibitory effect on root growth of Lemna minor or Spirodela polyrhiza
order to fully address these interactions and their consequences. duckweeds. Although all MnP used in these studies adhered to the roots
ii. Primary producers and leaves, it was only the larger primary PE particles (71.30 ± 34.29
Photosynthetic activity was one of the most common endpoints μm, 96.00 ± 69.99 μm and 180.5 ± 118.7 μm) extracted from facewash
measured when assessing effects on primary producers (19 out of 26 that showed a statistically significant inhibitory effect on the root length
studies). 3 out of 4 studies on the vascular-plant duckweed included this of L. minor (Kalčíková et al., 2017, Kalčíková et al., 2020). Leachate
endpoint. From these, all reported no significant effect, even at high effects were accounted for, suggesting that the microplastics themselves
exposure concentrations, such as 5 x104 PE particles mL− 1 (Mateos- caused some type of physical inhibitory effect at all tested concentra
Cárdenas et al., 2019). Photosynthetic activity was measured as tions (0.01, 0.05, and 0.1 mg mL− 1) (Kalčíková et al., 2017). This effect
chlorophyll-a (Chl-α) content with fluorometry (Mateos-Cárdenas et al., could be due to the MnP size or morphology, as the other MnP tested, i.
2019) and as chlorophyll pigment content with UV-VIS spectroscopy e., PE (10–45 μm at 5 × 104 particles mL− 1) (Mateos-Cárdenas et al.,
(Dovidat et al., 2020; Kalčíková et al., 2017). Contrary to this, the ma 2019) and PS (50 and 500 nm at 1 × 106 particles mL− 1) (Dovidat et al.,
jority of studies showed a significant effect of MnP on algal photosyn 2020), had more regular morphology, whereas the PE extracted from
thetic activity. Sjollema et al. (2016) measured the photosynthetic facewash was highly irregular. More studies are required with growth as
activity in C. vulgaris with Pulse Amplitude Modulation (PAM) fluo a unifying endpoint, so that the effect of morphology and plastic type
rometer after exposure to high concentrations of PS particles (500 nm at can be explored and clear comparisons made to establish what MnP
2.5 × 10− 2, mg mL− 1) and found no conclusive impact. Interestingly, features affect growth.
four other studies on cyanobacteria and freshwater algae Microcystis 8 out of 15 studies on freshwater algae measuring growth reported a
aeruginosa, S. obliquus and C. reinhardtii exposed to high PS particle clear inhibitory effect after exposure to MnP. For instance, effects were
concentrations in similar size-ranges (50 nm at 3.4 × 10− 3 mg mL− 1, induced by PS particles (70 nm at 1 mg mL− 1 and 500 nm at 0.05 mg
200 nm at 0.01 mg and 0.02 mg mL− 1, 70 nm at 0.1 mg mL− 1 and mL− 1) on S. obliquus and C. vulgaris, (Besseling et al., 2014; Tunali et al.,
300–600 nm at 0.1 mg mL− 1) showed decreased Chl-α content when 2020), by a mix of polymethyl methacrylate (PMMA) and PS fragments
measured with UV-VIS spectroscopy (Besseling et al., 2014; Feng et al., (<250 μm at 1.25 × 10− 2 mg and 0.125 mg mL− 1) on Scenedesmus sp and
2020; Zhang et al., 2018) and with a portable plant efficiency analyser Microcystis panniformis (Cunha et al., 2019) and by polyurethane (PUF)
(Li et al., 2020c). Conversion between mass and particle numbers was foam fragments (3 mm at 1.6 mg mL− 1) and its leachates on C. vulgaris
not possible in these cases and it is possible that the observed effects are (Luo et al., 2019a).
related to the MnP sizes and concentrations, or are species specific. The Lagarde et al. (2016) reported decreased growth of the algae
difference in method should not affect the outcome parameter (effi C. reinhardtii after exposure to PP fragments (400 < 1000 μm at 100 mg
ciency of photosynthetic activity), as UV -VIS Spectroscopy (Lich no volume reported), but only after 78 days. This, in conjunction with
tenthaler, 1987) and fluorometry can both be used to estimate the results from Mao et al. (2018), who reported that initial growth inhi
chlorophyll content of plants (Maxwell and Johnson, 2000). In order to bition of Chlorella pyrenoidosa exposed to PS particles (0.1 μm at 0.01,
obtain baseline data, experiments with different plastic types with spe 0.05 and 0.1 mg mL− 1), was countered after 22 days with biomass
cific sizes and concentration ranges should be repeated on different showing recovery, indicating some degree of organism adaptability.
species of algae. Photosynthetic activity appears to be a universally used This strongly suggests that longer exposure times are required when
endpoint for MnP toxicity tests and should continue being used to aid assessing the impacts of MnP on algal communities, as negative effects
future comparability of studies. seen at short exposure times might decrease in intensity over time or
Another common toxicity endpoint included for primary producers is vice versa.
growth (i.e., OECD, 2006, 2011, 2014b) which is relatively easy to It is thus suggested that growth measured as length of roots and
measure. Only 2 out of 4 vascular-plant based studies reported an leaves for plants and as algae biomass and/or cell densities should be
8
included as a principal endpoint. Other endpoints such as stress re crucial that the exposure times of primary producers will be extended.
sponses and gene regulation should be included, where feasible, as For example, the duration of exposure in D. magna and other cladocerans
explorative variables. This minimum toxicity endpoint reporting will species is usually 48 h for acute, and 21 days for chronic toxicity tests,
help to ensure that meta-analysis can be carried out in the future, according to OECD guidelines. However, it has been reported that some
leading to deeper understanding of MnP toxicity and the characteristics acute toxic effects (such as immobilisation) of D. magna and D. pulex are
responsible. not always obvious after 48 h (Jaikumar et al., 2018; Rehse et al., 2016),
iii. Primary consumers and life-time exposures have revealed higher toxicity than that at 24 h
Mortality is a common endpoint, determined often as the LC50 (lethal exposure (Kelpsiene et al., 2020), suggesting that acute exposure should
concentration required to kill 50% of the test population) or LD50 (lethal be extended to at least 72 h. Indeed, the OECD toxicity test guidelines
dose required to kill 50% of the test population). Most studies reported are currently being revised for use with nanoparticles (Nasser and
mortality if it occurred, or used alternative indirect mortality endpoints, Lynch, 2019).
such as immobilisation for cladecorans to estimate EC50 (half maximal A secondary endpoint for primary consumers should be reproduction
effective concentration, which is halfway between baseline and and where possible, multigenerational studies should be carried out.
maximum observed effect) (OECD, 2004). Where mortality was re This is required to improve our understanding on population level ef
ported, higher exposures seemed to be more lethal. For example, some fects. For example, three studies using non-disclosed proprietary type
studies reported little to no mortality in D. magna. when exposed to PS polymer from Cospheric LLC (1–5 µm), which measured reproduction
particles (51 nm at 0.1 mg mL− 1 and 1 µm at 1.25 × 10− 4 mg mL− 1) capacity in cladocerans Daphnia spp., all reported negative effects
(Chae et al., 2018; De Felice et al., 2019), whereas, some PS exposures (Jaikumar et al., 2019; Ogonowski et al., 2016; Pacheco et al., 2018). In
with similar size ranges did induce mortality (52 nm at 50 mg mL− 1 and addition, Felten et al. (2020), showed that PE 1–4 μm at 1 × 10− 3 mg
100 nm at 0.0863 mg mL− 1) (Mattsson et al., 2017; Reynolds et al., mL− 1 had a negative effect on reproduction of D. magna while a trans
2019). Another discrepancy was observed in the case of the crustacean generational study by Martins and Guilhermino (2018) showed that
H. azteca, whereby Panko et al. (2013) reported no mortality after D. magna went extinct in just two generations after exposure to
exposure to tyre and road wear fragments (<150 μm at 1 × 104 mg Kg− 1) Cospheric LLC (1–5 µm). It is clear that these specific MnP can have
over 41 days, while Khan et al. (2019) observed mortality of H. azteca population level effects on cladocerans, and this type of systematic
when exposed to tyre rubber alone (<500 μm at 3426 fragments mL− 1) testing is required on other types of plastics and species. Furthermore,
over 21 days. Here, the differences between mode of exposure, the multigenerational studies should be a considered for primary con
rubber types, associated additives and/or the road mixture could affect sumers, as otherwise the population level effects may be overlooked
toxicity. It is noted, that in order to better understand the toxicity (Martins and Guilhermino, 2018). Most primary producers have a short
mechanisms, food should always be provided, so that effects of starva life-cycle, making them ideal for this type of work.
tion would not be confused with those arising from the exposure Including these two principal toxicity parameters (growth and
(Aljaibachi et al., 2020). Furthermore, mortality should always be mortality) into each primary consumer MnP study is imperative. Con
recorded and if no mortality is observed, this should be clearly stated. siderations should be given to inclusion of secondary endpoints
Growth as an endpoint can reveal differences in toxicity of plastic (reproduction and multigenerational studies). Other, especially sub-
types and aid comparisons between biotic groups. For example, the lethal parameters, such as enzyme activities for oxidative stress or im
crustacean Gammarus pulex showed a significant reduction in growth mune response (e.g., Li et al., 2020d; Scopetani et al., 2020), should also
when exposed to PS fragments (20–500 μm at 10% of sediment) despite be explored, to expand our understanding of MnP toxicity and their
feeding activity not being affected (Redondo-Hasselerharm et al., 2018). modes of action.
Reduction in growth was also observed in G. fossarum, by Straub et al. iv. Secondary consumers
(2017), when exposed to PMMA and polyhydroxybutyrate (PHB) frag For secondary consumers, similar principal endpoints as for primary
ments (32–63 µm, 63–125 µm, and 125–250 µm at 1 × 105 fragments consumers should be included (growth, mortality and reproduction).
individual− 1), despite no effects on feeding rates. However, G. pulex did However, as secondary consumers develop much slower than primary
not exhibit growth inhibition when exposed to car tyre rubber of similar consumers, it is not always possible to include all three principal end
size and concentration (66 μm at 10% of sediment), despite retention points in one study, and therefore a combination of any two principal
times higher than for PS particles (Redondo-Hasselerharm et al., 2018). endpoints is acceptable. Still, as only one study from the reviewed
Similarly Panko et al. (2013) reported only slight non-statistically sig literature reported increased mortality of adult zebrafish exposed to PP
nificant inhibition in growth of Diptera Chironomus dilutus exposed to particles (~70 μm at 0.01 mg mL− 1) (Lei et al., 2018), further sub-lethal
tyre and road wear fragments < 150 μm at 1 × 104 mg Kg− 1 while endpoints should be included. Effects observed in secondary consumers
C. riparius and C. tepperi, were effected when exposed to PE (32–63 μm at include changes in histopathology, gene expression and behaviour (e.g.,
1259 mg Kg− 1 63–250 μm and 125–500 μm at 1 × 104 mg Kg− 1) (Silva Chae et al., 2018; Lei et al., 2018; Limonta et al., 2019; Oliveira et al.,
et al., 2019) and PE (1–4, 10–27, 43–54 and 100–126 μm each at 500 2013; Rochman et al., 2017; Wen et al., 2018). Therefore, for secondary
particles Kg− 1) (Ziajahromi et al., 2018). However, whether the car tyre endpoints we recommend assessment of behavioural changes (e.g.,
and road wear fragments are less toxic than other MnP, such as PS, PE, predatory performance or distance swam), acetylcholinesterase (AChE)
PMMA and PHB remains inconclusive. For example, Panko et al. (2013) activity, which is an important enzyme that catalyses the breakdown of
reported no effect on growth of the crustacean H. azteca exposed to tyre acetylcholine (neurotransmitter), or measures of oxidative stress,
and road wear fragments of size < 150 μm at 1 × 104 mg Kg− 1 while namely ROS or CAT (catalase gene) and SOD (superoxide dismutase).
Khan et al. (2019) observed negative effects on growth in H. azteca when One or more of these endpoints are encouraged to be included in future
exposed to tyre rubber of size < 500 μm at 3.426 × 103 fragments mL− 1. studies, to increase inter-comparability.
The difference observed could be driven by either the road pavement, Behavioural changes can be used as a measure of sub-lethal effect in
rubber types and associated specific mixture of additives and/or size, biota. This can be recorded using video combined with imaging software
dose and/or mode of exposure, suggesting that more systematic studies such as ImageJ (Chae et al., 2018; Critchell and Hoogenboom, 2018; da
are needed to determine the specific drivers of toxicity. To ensure Costa Araújo et al., 2020) or more sophisticated tools and programs that
comparability of effects across plastic types and species, growth, have been designed for behavioural tracking of fish, such as DanioVision
measured as weight and length or biomass should be included as an and EthoLog (Chen et al., 2017; Ottoni, 2000; Pedersen et al., 2020). For
endpoint for primary consumers. This will aid further meta-analysis and example, Chae et al. (2018) found that locomotive activity of two fish
species sensitivity analysis in the future. species, rice fish Oryzias sinensis and dark chub Zacco temminckii, were
Besides inclusion of the primary endpoints mentioned above, it is affected by PS particles (51 nm at 5 × 10− 3 mg mL− 1). It was also
9
reported that the livers of Z. temminckii showed abnormal histological This review has outlined some of the key recommendations and
patterns. Wen et al. (2018) similarly found that predatory performance reporting guidelines for field and laboratory studies, with the goal of
of discus fish Symphysodon aequifasciatus declined following exposure to increasing inter-comparability across studies and trophic levels. It is
PE particles (70–88 μm at 2 × 10− 4 mg mL− 1). This study also reported imperative that baseline studies on the parameters suggested in this
sub-lethal effects, such as a decrease in activity of enzymes AChE and review are systematically undertaken. Only by gathering this type of
Trypsin. It should be noted that these types of behavioural parameters data, can a full meta-analysis and comprehension of the effects of MnP
(such as predatory performance or distance swam) cannot explain the on freshwater ecosystems be produced.
underlying mode of action, however, they can offer important insight
into MnP effects and are encouraged to be monitored where possible. Credit authorship contribution statement
Neurotransmitter AChE decreased in 5 out of 6 studies assessed in
this review, indicating neurotoxicity for the tested plastic types (PE and Anna Kukkola: Conceptualization, Investigation, Methodology,
PS). PE was found to affect juvenile discus fish S. aequifasciatus (PE Formal analysis, Visualization, Writing - original draft, Reviewing and
70–88 μm at 2 × 10− 4 mg mL− 1) and streaked prochilod Prochilodus editing. Stefan Krause: Conceptualization, Funding acquisition,
lineatus (PE 10–90 μm at 2 × 10− 5 mg mL− 1) (Roda et al., 2020; Wen Writing - reviewing and editing, Supervision. Iseult Lynch: Conceptu
et al., 2018). Two separate studies on juveniles of the common goby alization, Funding acquisition, Writing - reviewing and editing, Super
Pomatoschistus microps reported similar effects on AChE when exposed to vision. Gregory H. Sambrook Smith: Conceptualization, Funding
PE (1–5 μm at 1.84 × 10− 5 mg mL− 1 and 1.84 × 10− 4 mg mL− 1) (Fonte acquisition, Writing - reviewing and editing, Supervision. Holly Nel:
et al., 2016; Oliveira et al., 2013). PS 0.1 μm also decreased AChE in red Conceptualization, Visualization, Writing - reviewing and editing,
tilapia Oreochromis niloticus at exposure concentrations of 1 × 10− 6, 1 × Supervision.
10− 5 and 1 × 10− 4 mg mL− 1 (Ding et al., 2018). Only LDPE (~10.9 μm)
at exposure concentrations of 5 × 10− 6, 5 × 10− 5, and 5 × 10− 4 mg mL− 1 Declaration of Competing Interest
showed no effect on AChE mRNA levels of zebrafish larvae (Karami
et al., 2017b). The duration of exposure is unlikely to explain these The author declare that there is no conflict of interest.
differences, as the studies that showed effects on AChE ranged from 96 h
to 31 days and the study of Karami et al. (2017b) exposed the larvae for
Acknowledgements
20 days, which falls within the range above. Whether the observed effect
on AChE levels was species specific, related to the age of exposed fish,
The authors would like to extend their gratitude towards Chantal
and/or plastic type is unclear. Inclusion of this endpoint where possible
Jackson and Dr. Giulio Curioni for their assistance with the graphics and
will facilitate assessment of possible neurotoxicity of different plastic
figures, and the three anonymous reviewers and the editor for their
types in different species.
critical reading of the manuscript and insightful suggestions that led to
Another important sub-lethal endpoint for secondary consumers is
the improvement of the manuscript. SK and IL are supported by the
oxidative stress, which can lead to tissue damage and disrupt cellular
Institute of Global Innovation at Birmingham University.
functions (Valavanidis et al., 2006). There is already evidence that some
MnP can induce oxidative stress in secondary consumers. For example,
CAT gene, that is related to the presence of oxidative stress, was upre Funding
gulated in zebrafish after exposure to PS particles (1 μm, 5 μm and 70
nm) at 1 × 10− 3 mg mL− 1 (Qiang and Cheng, 2019), 2 × 10− 4 or 2 × This work was supported by the Leverhulme Trust grant “Plasti
10− 3 mg mL− 1 (Lu et al., 2016). However, we recommend that more cRivers”- The fate and transport of microplastics in rivers (RPG-2017-
than one parameter for oxidative stress should be measured, as this can 377).
give an indication of whether biota can induce protective action against
ROS. For example, Parenti et al. (2019) showed that while PS (0.5 μm at Appendix A. Supplementary material
1 × 10− 3 mg mL− 1) induced activity of SOD it did not induce ROS. This
could indicate that high SOD activity in zebrafish could protect it from Supplementary data to this article can be found online at https://doi.
excessive ROS. This is supported by a study on red tilapia O. niloticus org/10.1016/j.envint.2021.106504.
exposed to 1 × 10− 6, 1 × 10− 5 and 1 × 10− 4 mg mL− 1 PS particles (0.1
µm), where particles induced SOD but did not affect malondialdehyde References
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Environment International 152 (2021) 106504

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Nano and microplastic interactions with freshwater biota – Current

Fig. 1. Conceptual model for MnP movements in the

studies, it is recommended to extend laboratory effect testing to a more

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