Science of the Total Environment 645 (2018) 1029–1039

Contents lists available at ScienceDirect

Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Review

Studies of the effects of microplastics on aquatic organisms: What do we

know and where should we focus our efforts in the future?
Luís Carlos de Sá a, Miguel Oliveira b, Francisca Ribeiro c, Thiago Lopes Rocha d, Martyn Norman Futter a,⁎
a
Swedish University of Agricultural Sciences, Uppsala, Sweden
b
University of Aveiro, Department of Biology, CESAM, Portugal
c
Queensland Alliance for Environmental Health Sciences, University of Queensland, Brisbane, QLD, Australia
d
Laboratory of Environmental Biotechnology and Ecotoxicology, Institute of Tropical Pathology and Public Health, Federal University of Goiás, Goiás, Brazil

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Mismatch between microplastics (MP)

in the environment and in ecotoxicol-
ogy studies
• Fish and small crustaceans are over-
represented in studies of MP effects
• Most lab studies are conducted at unre-
alistically high MP concentrations
• Mechanisms of MP action on organism
health still poorly understood

a r t i c l e i n f o a b s t r a c t

Article history: The effects of microplastics (MP) on aquatic organisms are currently the subject of intense research. Here, we pro-
Received 4 April 2018 vide a critical perspective on published studies of MP ingestion by aquatic biota. We summarize the available re-
Received in revised form 16 July 2018 search on MP presence, behaviour and effects on aquatic organisms monitored in the field and on laboratory
Accepted 16 July 2018
studies of the ecotoxicological consequences of MP ingestion. We consider MP polymer type, shape, size as well
Available online 20 July 2018
as group of organisms studied and type of effect reported. Specifically, we evaluate whether or not the available lab-
Editor: D. Barcelo oratory studies of MP are representative of the types of MPs found in the environment and whether or not they have
reported on relevant groups or organisms. Analysis of the available data revealed that 1) despite their widespread
Keywords: detection in field-based studies, polypropylene, polyester and polyamide particles were under-represented in labo-
Microplastic ratory studies; 2) fibres and fragments (800–1600 μm) are the most common form of MPs reported in animals col-
Ecotoxicology lected from the field; 3) to date, most studies have been conducted on fish; knowledge is needed about the effects of
Aquatic organisms MPs on other groups of organisms, especially invertebrates. Furthermore, there are significant mismatches between
the types of MP most commonly found in the environment or reported in field studies and those used in laboratory
experiments. Finally, there is an overarching need to understand the mechanism of action and ecotoxicological ef-
fects of environmentally relevant concentrations of MPs on aquatic organism health.
© 2018 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license
(http://creativecommons.org/licenses/by/4.0/).

⁎ Corresponding author.
E-mail address: martyn.futter@slu.se (M.N. Futter).

https://doi.org/10.1016/j.scitotenv.2018.07.207
0048-9697/© 2018 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
1030 L.C. de Sá et al. / Science of the Total Environment 645 (2018) 1029–1039

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1030
2. Methodological approach . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1031
3. Results and discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1031
3.1. Types of MPs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1031
3.1.1. Types of MPs and target groups reported in field and laboratory studies . . . . . . . . . . . . . . . . . . . . . . . . . . . 1031
3.1.2. Reports of organisms exposed to MPs in field and laboratory conditions . . . . . . . . . . . . . . . . . . . . . . . . . . . 1032
3.2. Ecotoxicological research on MPs. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1033
3.2.1. Organism groups used in ecotoxicological studies with MPs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1033
3.2.2. Ecotoxicological effects of MPs on aquatic organisms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1033
3.2.3. Interactive ecotoxicological effects of MPs with other contaminants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1035
4. Conclusions and future perspectives. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1036
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1036
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1036

1. Introduction
There is increasing scientific and societal concern about the
effects of microplastics (MPs), commonly defined as plastic particles
with sizes below 5 mm (Betts, 2008; Fendall and Sewell, 2009;
Hidalgo-Ruz et al., 2012), on freshwater and marine organisms
(Kubota, 1994; Gregory and Ryan, 1997; Yoon et al., 2010; Zarfl
and Matthies, 2010; Kako et al., 2011, 2014; Maximenko et al.,
2012; Isobe et al., 2014).
Microplastics can be classified as primary or secondary, depend-
ing on the manner in which they are produced. Primary MPs are
small plastic particles released directly into the environment via
e.g. domestic and industrial effluents, spills and sewage discharge
or indirectly (e.g. via run-off). The range of primary MP particle
types include fragments (Rummel et al., 2016), fibres (Rummel
et al., 2016), pellets (Nobre et al., 2015), film (Kang et al., 2015;
Lusher et al., 2015) and spheres (Li et al., 2016). Spheres are fre-
quently associated with pharmaceutical and cosmetics industries
(Zitko and Hanlon, 1991; Patel et al., 2009). Secondary MPs are
formed as a result of gradual degradation/fragmentation of larger
plastic particles already present in the environment, due to e.g. UV
radiation (photo-oxidation), mechanical transformation (e.g.
waves abrasion) and biological degradation by microorganisms
(Browne et al., 2007; Andrady and Neal, 2009; Cole et al., 2011).
Microplastics in the environment can be further degraded/
fragmented to produce nanoplastics (1–100 nm), which, when com-
pared to other forms of plastic litter, have largely unknown fates and
toxicological properties (Koelmans et al., 2015; da Costa et al., 2016).
The amount of MPs in the aquatic environment continues to in-
crease, in part due to ongoing increases in the production of plastics,
with a total global production of 335 M ton in 2016 (Plastics Europe,
2017). There are a number of characteristics (e.g. resistance to corro-
sion, low thermal and electrical conductivity, durability, ability to trans-
port other materials and low production cost) that make plastics
suitable for use in a wide variety of applications, from construction to
medicine (Bockhorn et al., 1999). These same characteristics
highlighted above make the presence of plastics in the environment
problematic. Furthermore, plastics may incorporate additional
chemicals during manufacture (Andrady and Neal, 2009; Fries et al.,
2013) which are added to endow them with specific characteristic but
which may be toxic if ingested. Chemicals may also be incorporated/
adsorbed by plastics in the environment (Zarfl and Matthies, 2010;
Velzeboer et al., 2014). Microplastic particles have a large surface area
to volume ratio which provides a high association potential for environ-
mental contaminants including polycyclic aromatic hydrocarbons
(PAHs) (Rios et al., 2007) or metals (Betts, 2008; Ashton et al., 2010).
There are a wide range of plastic polymers which are produced and
released to the environment. In Europe, polyethylene (PE) comprised
28%, polypropylene (PP) 19%, polyvinylchloride (PVC) 10% and polysty-
rene 7% of total production (Plastics Europe, 2017). Different plastic
polymers have a wide range of densities (from 16 to 2200 kg m−3;
Nizzetto et al., 2016) which influences MP behaviour in the aquatic en-
vironment. Furthermore, MPs are found in a wide range of shapes (e.g.
spheres, fibre, film, irregular). Differences in shape and density cause
MPs to disperse diversely in different compartments of the aquatic envi-
ronment (water surface, water column and sediment) and influence
their availability to organisms at different trophic levels and/or occupy-
ing different habitats (Betts, 2008; Thompson et al., 2009; Cole et al.,
2011). For example, pelagic organisms such as phytoplankton (Long
et al., 2015) and small crustaceans (e.g. zooplankton) (Desforges et al.,
2015) are more likely to encounter less dense, floating MPs while ben-
thic organisms including amphipods (Thompson et al., 2004), poly-
chaete worms (Mathalon and Hill, 2014), tubifex worms (Hurley et al.,
2017), molluscs (Brillant and MacDonald, 2002; Browne et al., 2008)
and echinoderms (Hart, 1991; Graham and Thompson, 2009) are
more likely to encounter MPs that are more dense than water. Both ben-
thic (de Sá et al., 2015) and pelagic (Rummel et al., 2016) fish may in-
gest MPs directly, or indirectly (i.e. consume them in prey). Birds
(Herzke et al., 2016) and mammals (Fossi et al., 2012) feeding on
aquatic organisms or living in aquatic environments are also known to
ingest MPs. Microplastics are found in almost all marine and freshwater
environments and have been detected in protected and remote areas
(Claessens et al., 2013) making their potential pernicious effects a global
problem.
To date, reviews on MPs in the environment have focused on
summarizing properties (e.g. Karimi, 2017), sources, fate and occur-
rence (e.g. Cole et al., 2011; Andrady, 2011; do Sul and Costa, 2014;
Auta et al., 2017; Cesa et al., 2017; Horton et al., 2017), concentra-
tions (Horton et al., 2017), analytical methods (e.g. Cole et al.,
2011; Hong et al., 2017) and effects on organisms (e.g. Cole et al.,
2011; Wright et al., 2013b; Auta et al., 2017; Cesa et al., 2017;
Horton et al., 2017).
Despite the available reviews concerning environmental concen-
tration and ecotoxicological impact of MPs on aquatic organisms
(e.g. Cole et al., 2011; Andrady, 2011; Barboza and Gimenez, 2015;
Anbumani and Kakkar, 2018; Rezania et al., 2018), there is a lack of
critical evaluation of the current research trends related to types of
MPs detected in aquatic animals versus the type of MP and study or-
ganism used in laboratory studies of ecotoxicological effects (Phuong
et al., 2016; Horton et al., 2017). Thus, this paper aims to: (i) summa-
rize and discuss the current field and laboratory research trends in
terms MP polymer type, shape and size reported and organism
group studied; (ii) critically review the published studies of ecotox-
icological effects of MPs on freshwater and marine biota with respect
to the aforementioned criteria and (iii) identify promising areas for
future research.
 L.C. de Sá et al. / Science of the Total Environment 645 (2018) 1029–1039
2. Methodological approach
A survey of the available published peer-reviewed literature was
conducted on November 22, 2017 through a bibliographic study
using the Thompson Reuters database ISI Web of Science. A combina-
tion of keywords was used as criteria (i.e. “microplastic*”, in any
topic, title or text words). A total of 1637 candidate publications
were identified. The abstracts of all candidate articles were read so
as to identify relevant field or laboratory studies reporting on MP in-
gestion or ecotoxicological effects in marine or freshwater aquatic
animals. Of the 1637 candidate publications, 157 were retained for
further analysis. Available studies were summarized according to
the following criteria: (i) type of MPs used and/or reported; (ii)
shape of MP used and/or reported; (iii) MP size range; (iv) group
of organisms studied; and (v) type of ecotoxicological effect
observed.
The following list of plastic types was used to classify MP parent ma-
terials reported in the literature: polyethylene (PE), polystyrene (PS),
polypropylene (PP), polyester (PES), polyvinylchloride (PVC), polyam-
ide (PA), acrylic polymers (AC), polyether (PT), cellophane (CP), poly-
urethane (PU) and not specified (NS). The PE family includes both
high- and low-density PE and PES plastics such as polylactic acid and
polyethylene terephthalate. The selected plastic types include the
main groups of MP parent materials reported in e.g. Plastics Europe
(2017).
When specified, shapes of MPs were classified according to the fol-
lowing list: spheres, fibres, fragments, film, and pellets. Microplastic
size was assigned to one or more of the following classes: b50 μm
(including nanoplastics); 50–100 μm; 100–200 μm; 200–400 μm;
400–800 μm; 800–1600 μm; N1600 μm; or not specified (NS).
The groups of organisms studied included the following: fish, birds,
amphibians, reptiles, mammals, large crustaceans, small crustaceans,
molluscs, annelid worms, echinoderms, cnidaria, rotifera and porifera.
‘Small crustaceans’ included zooplankton while ‘large crustaceans’ in-
cluded all other crustacean taxa. Plants and microbes were not included
in the results reported here.
Ecotoxicological effects enumerated included mortality, reproduc-
tive impairment, neurotoxicity, biotransformation of enzymes,
genotoxicity, physical effects, behavioural effects, oxidative stress and
damage, cytotoxicity, blood/haemolymph effects and increased accu-
mulation of other contaminants. No attempt was made to separate di-
rect ecotoxicological effects from e.g. organism responses associated
with starvation following MP ingestion.
The information in every article was tabulated and summarized
in the following manner: An article could report one or more studies.
A study was defined as a series of observations of one group of organ-
isms, type of MPs, shape and/or size. Any article reporting data on
more than one of the aforementioned categories generated a number
of studies equal to the number of elements per premise. For example,
if one article reported only on fish it was considered to be one study,
but if it reported on both fish and large crustaceans, it was consid-
ered to be two studies. Similarly, if one article only reported effects
of PE MP, it was considered to be one study, but if it documented
effects of both e.g. PE and PS MPs in fish and small crustaceans it
was considered to be four studies. Thus, the number of studies
presented in the results represents the number of interactions of
the aforementioned classification criteria (organism group, MP
type, MP shape, MP size), not the total number of publications.
Our search identified 157 published, peer-reviewed articles
which documented a total of 612 studies (listed in supplementary
information). In Sections 3.2.1–3.2.3 where MPs effects are
described, only studies which report MP effects on organisms were
considered. Thus, a number of studies of interactive effects of MPs
and other contaminants for which no impacts of MPs were identified
during our review of candidate literature have not been included
here.
1031
3. Results and discussion
3.1. Types of MPs
3.1.1. Types of MPs and target groups reported in field and laboratory
studies
The types of MPs most commonly reported across field and labora-
tory studies include PE (23%) and PS (22%), followed by PP (12%) and
PES (9%) (Fig. 1). Fish were the most commonly studied group of organ-
isms (44%), followed by crustacea (21% for large and small crustacea
combined), molluscs (14%) and annelid worms (6%) (Fig. 2). There
were relatively few studies of other organism groups.
Polyethylene was the most common type of MP studied in fish, it
was reported in 34 studies, or 12% of the total number of studies identi-
fied. Ingestion of PE by fish is both widespread and crosses habitat pref-
erences. For example, Lusher et al. (2013) showed that over one third of
fish examined in their study had ingested MPs, with pelagic and benthic
fish displaying similar gut contents, suggesting either a lack of selectiv-
ity or widespread presence of PE in both the water column and sedi-
ments. The presence of PE was reported less commonly in other
groups of organisms, with 12 studies on molluscs, seven on small crus-
taceans and four on annelids (Fig.2). There were relatively few studies
of PE in vertebrates other than fish. (Fig. 2).
Effects of PS MPs have been reported in studies of fish (n = 17) and
small crustaceans (n = 19) (Fig. 2). Although crustaceans have been
shown to have the ability to distinguish live particles from inert ones,
e.g. algae and PS beads (Poulet and Marsot, 1978), ingestion of PS MPs
has been observed in small crustaceans occupying both pelagic and ben-
thic environments. Taxonomic groups in which PS MPs were detected
include the marine copepods Acartia spp. and Eurytemora affinis
(Setälä et al., 2014), large crustaceans such as the estuarine mysid
Neomysis integer (Setälä et al., 2014) and the crab Uca rapax
(Brennecke et al., 2015). Cole et al. (2013) reported that dead copepods
can have adhered PS fragments, which could contribute to the vertical
transport of this type of MP. Nizzetto et al. (2016) report densities of
1040–1090 kg m−3 for PS and 910–940 kg m−3 for PE. These differences
may explain the discrepancy in the number of studies reporting PE MPs
in fish and other pelagic organisms versus the number of studies
reporting PS MPs in benthic fish and crustaceans. The density of PS
MPs is usually greater than PE MPs, so they may be available not only
in the water column, but also in the sediment (Browne et al., 2007),
representing a higher risk for both pelagic and demersal organisms,
while PE MPs have a lower density presenting a higher availability in
the water column and potentially pose a higher risk for pelagic fish
(Phuong et al., 2016). However, densities of these polymers may change
PE 61
PS 57
Types of Microplastics
NS 38
PP 31
PES 23
PVC 18
PA 17
AC 12
PT 2
CP 2
PU 1
0 5 10 15 20 25 30
% of studies
Fig. 1. Percentage of studies under the conjugation of the subjects “microplastics” and
“ingestion/effects on organisms” per type of microplastics. Every bar has total number of
studies. Studies were defined according to the typology of microplastics. Different types
of microplastics enumerated include PE-Polyethylene; PS-Polystyrene; NS-Not specified;
PP-Polypropylene; PES-Polyester; PVC-Polyvinylchloride; PA-Polyamide; AC-Acrylic; PT-
Polyether; CP-Cellophane; PU-Polyurethane.
1032 L.C. de Sá et al. / Science of the Total Environment 645 (2018) 1029–1039

50

% of the different types of

131 NS
45
PU
40
CP
microplastics 35
PT
30
AC
25 PA
20 PVC
15 40 39 PES
10 22 19 PP
5 11 10 9
5 5 PS
2 1 1
0 PE

Groups of organisms

Fig. 2. Percentage of the different type of microplastics per group of organisms. Every bar has the total number of studies. Studies were defined according the typology of microplastics and
the number of individuals per group of organisms. Plastic types enumerated include NS-Not specified; PU-Polyurethane; CP-Cellophane; PT- Polyether; AC-Acrylic; PA-Polyamide; PVC-
Polyvinylchloride; PES-Polyester; PP-Polypropylene; PS-Polystyrene; PE-Polyethylene.

while in the environment as a result of e.g. biofilms or flocculation contaminants, and its bioavailability (Andrady and Neal, 2009; Zarfl
(Rummel et al., 2017). and Matthies, 2010; Antunes et al., 2013; Fries et al., 2013; Oliveira
The widespread distribution of MPs in aquatic ecosystems (Lusher et al., 2013; Rochman et al., 2013; Velzeboer et al., 2014) and its effects
et al., 2013) and broad range of physicochemical properties makes a on organism health (Au et al., 2015; Straub et al., 2017).
wide range of aquatic organisms potentially susceptible to these emerg-
ing contaminants. There are a number of ways in which organisms may
accumulate MPs. Animals exposed to MPs may incorporate them
through their gills (Watts et al., 2014) and digestive tract (Boerger Fish 71
Field
Small Crustacea 36
et al., 2010; Denuncio et al., 2011; de Stephanis et al., 2013; Jantz Laboratory
Large Crustacea 15
et al., 2013; Lusher et al., 2013; Rebolledo et al., 2013; de Sá et al.,
Groups of organims

Mollusca 29
2015). The ingestion may be due to an inability to differentiate MPs Annelida 12
from prey (de Sá et al., 2015) or ingestion of organisms of lower trophic Mammalia 6
A
levels containing these particles (e.g. plankton containing MPs) Echinodermata 6
Birds 5
(Browne et al., 2008; Fendall and Sewell, 2009; do Sul and Costa,
Cnidaria 3
2014). MPs may also adhere directly to organisms (Dabrunz et al., Rotifera 2
2011; Cole et al., 2013). Amphibia 1
Reptilia 1

3.1.2. Reports of organisms exposed to MPs in field and laboratory Porifera 1

conditions 0 5 10 15 20 25 30 35 40 45
Despite the ever increasing number of studies of the effects of MPs % of studies
on aquatic biota, there is a possibility that effect studies may be biased Fish 71
Freshwater
towards to a particular type of polymer without due consideration of re- Small Crustacea 36
ported occurrence in organisms and the environment, estimated release Large Crustacea 15 Seawater
Groups of organims

to the environment and bioavailability. The same possibility should also Mollusca 29
Annelida 12
be considered for the model organisms used in laboratory assays.
Mammalia 6
The surveyed publications identified an equivalent number of stud- B
Echinodermata 6
ies conducted in the field (48%) and laboratory (52%) (Fig. 3A). How- Birds 5
ever, there are differences in the groups of organisms studied. Fish are Cnidaria 3

the most studied organism group in the field (23% of all studies), Rotifera 2

whereas small crustaceans are the group most studied in the laboratory Amphibia 1
Reptilia 1
(17% of all studies) (Fig. 3A). Such differences may be the result of diffi- Porifera 1
culties in maintaining and handling large and/or long-lived organisms
0 5 10 15 20 25 30 35 40 45
under controlled conditions. Unfortunately, a sizeable fraction of the
% of studies
field studies (24%) did not report the typology of MPs present in the
biota (Fig. S1). This is a highly relevant shortcoming considering that
Fig. 3. Field and laboratory exposures (A) and Freshwater and seawater organisms (B) in
the properties of the MP parent material are likely to influence both the study of the ingestion and effects of microplastics. Every bar has the total number of
its physical behaviour in the environment (e.g. presence in the water studies. Studies were defined according the number of individuals per groups of
column or in sediments), the potential to adsorb environmental organisms.
 L.C. de Sá et al. / Science of the Total Environment 645 (2018) 1029–1039
The most common types of MPs reported in biota collected during
field sampling include PE (17%), PP (14%), PES (13%), PA (10%) and PS
MPs (9%) (Fig. S1). This detection frequency largely reflects rates of
plastic production, except that PS plastics are produced in greater
amounts than either PES or PA. While field studies generally reflect re-
ported plastic production rates, these polymers were not studied with
similar frequency in laboratory assays (Fig. S1). In fact, only 8% of the
laboratory studies have been performed with PP MPs whereas PS and
PE MPs were used in 40% and 33% of the studies respectively (Fig. S1).
It becomes apparent that there is a need for further laboratory studies
documenting the potential effects of PP MPs, considering that it is one
of the most produced and demanded types of plastic, with about 20%
of European production, much more than the 7% of production devoted
to PS (Plastics Europe, 2017).
The shape of MPs reported in organisms collected during field sur-
veys is varied. Fibres and fragments were reported in 23% and 21% of
studies, respectively, followed by spheres (11%), film (8%) and pellets
(4%) (Fig. S2). However, in laboratory studies, spherical MPs have
been the most commonly used shape (17%) followed by fibres, frag-
ments and unspecified particles (all 3%) (Fig. S2). From this, it can be
seen that there is a need to perform more laboratory studies with fibres
and fragments given their frequency of detection in animals collected
from the field and their widespread presence in the environment. The
MP size used or reported in published studies also varies and is related
to MP shape (Fig. S2), with almost every shape having been reported
across all size ranges (Fig. S2). The size ranges 800–1600 μm (12%)
and 400–800 μm (12%) were the most commonly reported in animals
collected from the field, followed by 200–400 μm (11%) (Fig. S2). In
the laboratory, smaller particles (b50 μm) were used most commonly
(75 / 169 laboratory studies where MP size was reported) (Fig. S2).
This may reflect the difficulty in sampling smaller particles from envi-
ronmental media as the size of MPs in biological samples collected in
the environment may be biased by sampling and detection methodol-
ogy that seem to contribute to the scarcity of reports of MP with a size
b 50 μm. The size range 800–1600 μm, the most commonly reported
from field samples of biota represents a very small fraction of the sizes
used in the laboratory (Fig. S2). This mismatch in size between field ob-
servations and laboratory studies demonstrates a clear research gap.
However, this discrepancy should be evaluated in light of the relative
distribution of MP size fractions reported in relevant compartments of
the aquatic environment including floating material and sediments.
3.2. Ecotoxicological research on MPs
The first studies concerning the potential ecotoxicological impact of
MPs on aquatic organisms were carried out in latter half of the 2000s by
Browne et al. (2008), who performed a laboratory study in which they
observed the translocation of MP particles from the gut to the circula-
tory system of Mytilus edulis. Since then, the total number of field and
laboratory studies involving MPs and their interactions and effects on
aquatic organisms has grown significantly, especially after 2012.
3.2.1. Organism groups used in ecotoxicological studies with MPs
To date, ecotoxicological studies of MPs have been conducted pre-
dominantly using marine (77%) as opposed to freshwater (23%) organ-
isms (Fig. 3B). This lack of ecotoxicological knowledge on the behaviour
of MPs in the freshwater environment has been commented on by a
number of authors (Eerkes-Medrano et al., 2015; Wagner et al., 2014;
Phuong et al., 2016). This knowledge gap is of high concern since fresh-
water organisms are directly affected by terrestrial runoff, wastewater
and other discharges potentially containing high levels of MPs and
other contaminants (Dris et al., 2015). Furthermore, they may encoun-
ter more highly contaminated sediments, increasing the likelihood of
synergistic effects of MPs with other environmental pollutants.
Among the reports of MPs in marine organisms, fish are the most
commonly studied group (25%), followed by molluscs (15%), small
1033
crustacea (11%), large crustacea (8%) annelid worms (6%), mammals
and echinoderms (both 3%), birds and cnidaria (both 2%), porifera, rep-
tiles and rotifers (all b 1%) (Fig. 3B). Multiple freshwater studies only
exist for fish (13% overall, 56% of the freshwater studies) and small crus-
tacea (8% overall, 35% of the freshwater studies). There are individual
studies of MPs in freshwater birds, amphibians, annelid worms and ro-
tifers (Fig. 3B). The relative paucity of ecotoxicological studies on groups
of organisms other than fish and small crustacea in freshwater environ-
ments highlights that the effects of MPs on freshwater ecosystems has
been under-studied and deserves further attention. Specifically, the ef-
fects of MPs on molluscs and freshwater benthic crustaceans is worthy
of further study as these groups of organisms may be exposed to high
levels of MPs in sediments (Nel et al., 2018).
To date, the most studied species in the laboratory has been the
small freshwater planktonic crustacean Daphnia magna (12%)
(Besseling et al., 2014; Booth et al., 2016; Jemec et al., 2016; Ma et al.,
2016; Nasser and Lynch, 2016; Ogonowski et al., 2016; Rehse et al.,
2016; Rist et al., 2016; Kim et al., 2017; Mattson et al., 2017; Aljaibachi
and Callaghan, 2018). The number of studies of D. magna may reflect
its widespread use in ecotoxicology laboratories.
Other commonly studied species include the freshwater fish Danio
rerio (7%) (Khan et al., 2015; Lu et al., 2016; Chen et al., 2017a, 2017b;
Sleight et al., 2017; Veneman et al., 2017; Lei et al., 2018), the common
goby, a marine fish Pomatoschistus microps (6%) (Oliveira et al., 2012,
2013; de Sá et al., 2015; Luis et al., 2015; Ferreira et al., 2016; Fonte
et al., 2016), a mollusc (the marine blue mussel M. edulis;5%) (von
Moos et al., 2012; Wegner et al., 2012; De Witte et al., 2014, Van
Cauwenberghe and Janssen, 2014, Van Cauwenberghe et al., 2015),
and the annelid lugworm Arenicola marina (5%) (Besseling et al., 2013;
Browne et al., 2013; Wright et al., 2013a; Van Cauwenberghe et al.,
2015; Green et al., 2016). Given the differences in habits and physiology
of marine and freshwater species, it is not clear to what extent results
based on studies of marine organisms can be applied to freshwater spe-
cies and vice versa. This further highlights the need for additional stud-
ies, especially in highly contaminated, low salinity environments such
as the Baltic where both marine and freshwater organisms are subject
to a high degree of environmental stress (Ojaveer et al., 2010).
Furthermore, closely related species may show differences in re-
sponse to MP exposure. Jaikumar et al. (2018) showed that three Daph-
nia species showed different responses to primary and secondary MP
exposure, and different interactive effects of MP exposure and thermal
stress. While the authors note that their study should be interpreted
with caution due to the High MP concentrations used, their results do
suggest a need for studies across a wider range of organisms than com-
monly used ecotoxicological model species such as D. magna and D. rero.
3.2.2. Ecotoxicological effects of MPs on aquatic organisms
A total of 130 studies reporting ecotoxicological effects of MPs on
aquatic organisms were identified (Fig. 4). Crustaceans were the most
commonly studied taxonomic group (45%), followed by fish (21%), mol-
luscs (18%), annelid worms (7%), echinoderms (7%) and rotifers (2%).
These organism groups occupy a number of positions in aquatic food
webs. Fish are generally intermediate/top predators (Oliveira et al.,
2012, 2013; Pochberger et al., 2014; de Sá et al., 2015) and may ingest
MPs either directly or through consumption of prey containing MPs.
Small crustaceans are often primary consumers (Desforges et al.,
2014), as are planktonic rotifers. Molluscs include a number of ecologi-
cally and commercially important filter feeding organisms. Because of
their habitat and feeding behaviour, molluscs and other benthic organ-
ism groups such as annelid worms are likely to be affected by MPs. Mol-
luscs include a large number of filter feeding species, with a high
tendency for bioaccumulation. Considering that several of these organ-
isms are widely used for food (e.g. M. edulis), they are a potential source
of MPs or environmental contaminants to humans (Wegner et al., 2012;
Van Cauwenberghe and Janssen, 2014). The relative lack of studies con-
ducted on other organism groups (e.g. vertebrates other than fish,
1034 L.C. de Sá et al. / Science of the Total Environment 645 (2018) 1029–1039
Mortality
Reproduction
Neurotoxicity
Biotransformation enzymes
Genotoxicity
14 9 5 10 29 7 2 7 1
100%
90%
80%
70%
60%
50%
40%
30%
20%
10%
0%
PE PS PVC PE PS PP PVC
Fish Crustacea
Fig. 4. Ecotoxicological effects of microplastics on the different groups of organisms. Every bar has the total number of studies. Studies were defined according to the type of MPs, groups of
organisms and effects.
echinoderms, cnidaria, rotifers and porifera) should be addressed as
these animals in these groups are likely to play an important role in
aquatic food webs (Fig. 3A,B). Specifically, studies targeting mode of ac-
tion (MoA) must be conducted to determine whether or not MPs have
similar effects on fish as they do on other vertebrate taxa, and whether
studies of small crustacea exposed to MPs provide sufficient insight into
ecotoxicological effects on other groups of invertebrates.
A range of ecotoxicological effects of different MP types have been
documented across several groups of organisms (Fig.4, Table S1). In
the following, the duration and/or type of experiment, size of MP and
concentration are reported for each study. Documented effects of PE
MPs in fish (Fig. 4) include neurotoxicity (96 h; 1–5 μm;
0.184 mg L−1) (Oliveira et al., 2012, 2013; Luis et al., 2015), reduction
of the predatory performance and efficiency in P. microps (predatory
test; 420–500 μm; 100 particles L−1) (de Sá et al., 2015). Mazurais
et al. (2015) reported mortality and induction of the cytochrome P450
(CYP P450) in D. labrax (846 h; 10–45 μm; 10–100 particles mg−1 of
diet). Polyethylene MPs have been shown to affect growth and repro-
duction of a large freshwater crustacean, the amphipod Hyalella azteca
(240 h and 1008 h; 10–27 μm; 0–108 particles L−1) (Au et al., 2015).
Several toxic effects related to immune response, oxidative stress and
genotoxicity have been reported in molluscs including a study of the
marine mussel Mytilus galloprovincialis exposed to PE MPs (168 h;
b100 μm; 20,000 mg L−1) (Avio et al., 2015). Van Cauwenberghe et al.
(2015) observed an increase of energy consumption by the polychaete
A. marina when exposed to PE MPs (336 h; b100 μm; 1.1 × 105
particles L−1). In echinoderms, PE MPs (120 h; 10–45 μm; 3 × 105
particles L−1) have been shown to influence larval growth and develop-
ment of Tripneustes gratilla without affecting its survival (Kaposi et al.,
2014). These results were corroborated by Nobre et al. (2015) for
Lytechinus variegatus larvae (24 h; 200 ml particles L−1). It is note-
worthy that these studies have all been conducted at MP concentra-
tions higher than those typically encountered in the aquatic
environment.
Effects of PP MPs on H. azteca (240 h and 1008 h; 20–75 μm; 0–9
× 104 particles L−1) have been reported by Au et al. (2015) who demon-
strated a higher toxicity for PP than PE MPs. They reported a LC50 = 7.14
× 104 particles L−1 for PP MPs compared to LC50 = 4.64 × 107
particles L−1 for PE MPs.
Physical effects
Behavior effects
Oxidative stress
Cytotoxicity
Blood and Hemolymph parameters
3 8 16 2 3 4 3 6 2
PES PA AC PE PS PE PS PVC PE PS PS
Mollusca Annelida Echinodermata Rotifera
Effects of PS MPs have been widely documented. In studies with the
fish D. rerio, PS MPs have been shown to be responsible for the up-
regulation of genes involved in the nervous and visual (Chen et al.,
2017a, 2017b) (48–120 h; 0.04–0.42 μm; 1 mg L−1) as well as immune
system (Veneman et al., 2017) (Injection; 0.7 μm; 5000 mg L−1). Studies
of small crustaceans include those by Cole et al. (2015) and Lee et al.
(2013) who observed a decrease in survival and fecundity of the marine
copepods Calanus helgolandicus (24 h and 216 h; 20 μm; 6.5–7.5 × 104
particles L−1) and Tigriopus japonicas (two generation test; 0.05–0.5
μm; 0.125–25 mg L−1) when exposed to PS MPs. Gambardella et al.
(2017) and Jeong et al. (2017) demonstrated some alteration of en-
zymes in the small crustaceans Artemia franciscana (48 h; 0.1 μm;
0.001–10 mg L−1) and Paracyclopina nana (24 h; 0.05–6 μm;
0.1–20 mg L−1). Avio et al. (2015) documented similar enzyme alter-
ation effects following PS and PE MP exposure in. the marine mollusc
M. galloprovincialis (168 h; b100 μm; 2 × 103 mg L−1). Additional eco-
toxicological effects of exposure to PS MPs was observed in two mollusc
species. A study using Scrobicularia plana (Ribeiro et al., 2017) reported
increases in neurotoxicity and genotoxicity. A 25% increase in energy
consumption was reported after ingestion of PS MPs by M. edulis
(336 h; b100 μm; 1.1 × 105 particles L−1) (Van Cauwenberghe et al.,
2015), probably associated with an effort to digest inert material and
maintain physiological homeostasis (von Moos et al., 2012). In
M. edulis, the transition of MP from the gut to the haemolymph was ob-
served to continue for N48 days after a 3 days exposure (Browne et al.,
2008). This persistence of MPs in mussel tissues represents a possible
source of toxicity to their predators and potentially to humans (e.g. De
Witte et al., 2014; Van Cauwenberghe and Janssen, 2014), and empha-
sizes the relevance of this topic of research. In the polychaete
A. marina ecotoxicological effects of exposure to PS MPs (672 h;
400–1300 μm; 105 mg L−1) include reduced feeding activity and reduc-
tion of lysosomal membrane stability (Besseling et al., 2013). Van
Cauwenberghe et al. (2015) also observed an increase of energy
consumption by A. marina when exposed to PS MPs (336 h; b100 μm;
1.1 × 105 particles L−1). Della Torre et al. (2014) described effects of
PS MPs (6–48 h; 0.04–0.05 μm; 1–50 mg L−1) on gene expression in
the echinoderm Paracentrotus lividus, including an up-regulation of
the Abcb1 gene responsible for protection and multi-drug resistance
(Shipp and Hamdoun, 2012). In rotifers, a decrease in growth rate and
 L.C. de Sá et al. / Science of the Total Environment 645 (2018) 1029–1039 1035

fecundity was observed following exposure to PS MPs (288 h; 0.05–6 fish (63%), with some studies of molluscs (19%), crustacea (14%) and an-
μm; 0.1–20 mg L−1) (Jeong et al., 2016). nelid worms (5%). Studies involving fish include e.g. (Oliveira et al.,
Studies with A. marina subject to sediment PVC exposure (48 h, 2012, 2013; Rochman et al., 2013; Chen et al., 2017a; Sleight et al.,
672 h; 130 μm; 5–50 × 103 mg of particles kg−1 of sediment) showed 2017; Rainieri et al., 2018). Crustaceans were studied by Watts et al.
a depletion of lipid reserves and an inflammatory response (Wright (2015) and Tosetto et al. (2016). Molluscs studies included e.g. (Avio
et al., 2013a). et al., 2015; Paul-Pont et al., 2016; Rist et al., 2016; Guilhermino et al.,
Overall, documented effects of MPs on aquatic organisms include re- 2018). Annelida were studied by Besseling et al. (2013). Unfortunately,
duction of feeding activity (Besseling et al., 2013; de Sá et al., 2015), ox- Herzke et al. (2016) did not specify the type of MP used in their study of
idative stress (Della Torre et al., 2014), genotoxicity (Della Torre et al., legacy POP accumulation in the seabird Fulmaris glacialis so it was not
2014), neurotoxicity (Oliveira et al., 2012, 2013; Luis et al., 2015; possible to include this study in Fig. 5.
Ribeiro et al., 2017), growth delay (Della Torre et al., 2014; Au et al., Studies examined the combined effects of MPs with legacy POPs
2015; Redondo-Hasselerharm et al., 2018), reduction of reproductive (64%), endocrine disrupting compounds (EDCs; 17%), metals (10%),
fitness (Lee et al., 2013; Au et al., 2015; Cole et al., 2015) and ultimately antibiotics (7%) and herbicides (2%). Legacy POPs included PAHs,
death (Lee et al., 2013; Au et al., 2015; Cole et al., 2015; Mazurais et al., polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers
2015; Li et al., 2016). (PBDEs) and dichlorodiphenyltrichloroethanes (DDT and break-
The MP concentrations used in sediment ecotoxicological studies are down products). Metals included silver, chromium VI and nickel. Ef-
of a similar order of magnitude to the highest field reported concentra- fects of MPs and the antibiotics celafaxin and triclosan as well as the
tions. Hurley et al. (2018) report maximum sediment concentrations of herbicide paraquat were documented. Endocrine disrupting com-
~440,000 particles m−2, and an average of 16,000 particles m−2. How- pounds included the pharmaceutical 17α-ethinylestradiol and
ever, concentrations of suspended MPs used in ecotoxicological studies Bisphenol-A. Slightly more than half the studies (54%) were con-
are generally higher than average surface water concentrations summa- ducted using PE MPs. Polystyrene (29%), PVC (19%) and PP (4%)
rized by Hurley et al. (2018). This is a significant concern as unrealisti- MPs were also reported.
cally high concentrations of MPs in experimental studies may lead to Adverse effects of MPs (PE; 1–5 μm; 0.184 mg L−1) with chromium
erroneous or misleading conclusions about the risks posed to aquatic (VI) (3.9 mg L−1) including neurotoxicity and mortality were reported
organisms. in a study of P. microps (Luis et al., 2015), suggesting that this metal
can adhere to MP surface and that populations from two estuaries can
3.2.3. Interactive ecotoxicological effects of MPs with other contaminants be differently influenced by this combined exposure (Luis et al., 2015).
There are a large number of studies on the combined effects of MPs Studies on the combined effects of MPs and POPs exposure include
with other environmental contaminants (Fig. 5, Table S2). These studies e.g. PCBs (Besseling et al., 2013; Rochman et al., 2013; Herzke et al.,
are motivated by the situation found in the environment where organ- 2016), DDT (Rios et al., 2007; Watts et al., 2015; Herzke et al., 2016)
isms are simultaneously exposed to several contaminants. The main and PAHs (Oliveira et al., 2012, 2013; Avio et al., 2015; Paul-Pont
goal of these studies is to investigate if MPs can interact positively or et al., 2016; Rist et al., 2016; Tosetto et al., 2016; Sleight et al., 2017;
negatively with the ecotoxicological effects of other contaminants. Batel et al., 2018). Both genotoxicity and reproductive effects were
There may be synergistic effects of MPs and other contaminants on or- often reported in this group of studies.
ganism health, or MPs may function as a transport vector for other Chen et al. (2017a) and Sleight et al. (2017) studied the interactions
contaminants. of MPs and the 17α-ethinylestradiol, a synthetic hormone which can
We identified 59 studies of interactive effects of other environmen- function as an EDC. They documented genotoxicity, reproductive and
tal contaminants with MPs (Fig. 5). Most studies had been performed on behavioural effects in the fish D. rerio.

Mortality Physical effects Reproduction

Behavioral effects Neurotoxicity Oxidative stress
Biotransformation enzymes Cytotoxicity Genotoxicity
Blood and Hemolymph parameters Oxidative damage Contaminant accumulation
2 11 3 3 3 3 1 4 4 1 2 2 1 1 2 2 4 5 2 2 1
100%
90%
80%
70%
60%
50%
40%
30%
20%
10%
0%
17α-ethinylestradiol
17α-ethinylestradiol
Paraquat
PAHs

Chromium VI

PCBs

PBDEs

PAHs

PAHs

PAHs

Nickel

PCBs

DDT, DDE

PAHs

PAHs

PAHs

PCBs
Silver

Cefalexin

Bisphenol A

Triclosan

PE PS PVC PE PS PP PE PS PVC PS PVC

Fish Crustacea Mollusca Annelida

Fig. 5. Combined ecotoxicological effects of MPs with other contaminants on the different groups of organisms. Every bar shows the total number of studies. Studies were defined according
to the type of MPs, groups of organisms and effects.
1036 L.C. de Sá et al. / Science of the Total Environment 645 (2018) 1029–1039
Browne et al. (2013) documented increased mortality of the annelid
worm A. marina exposed to PVC MPs and the antibiotic triclosan. Fonte
et al. (2016) showed a range of effects including neurotoxicity and
changes in enzyme activity when the fish P. microps was exposed to
PE MPs and the antibiotic celafaxin.
Accumulation of MP-associated contaminants (i.e. a “Trojan
Horse”) may result in an increase of the potential risk of contaminant
accumulation for higher trophic levels including humans (Oliveira
et al., 2013; Luis et al., 2015). The available data (Fig. 5) emphasizes
the negative effects of those interactions and reveals the importance
of studies focusing on the combined effects of MPs and other envi-
ronmental contaminants, after short and long-term exposure pe-
riods, since the consequences of these combinations are still poorly
known (Wright et al., 2013b). There is an absence of studies that as-
certain MPs capability to adsorb other contaminants once inside the
organisms, which may represent a positive outcome. However, there
are likely to be significant analytical challenges associated with
conducting such studies. Furthermore, there is a lack of information
about the interactive effects of MPs and other contaminants on
freshwater organisms. Considering that there are many freshwater
organisms with considerable trophic and commercial importance,
this approach should be one of the directions that the study of MPs
should take.
In our search there was only one article (Ferreira et al., 2016) that in-
dicates that MPs had no combined effects with the other tested contam-
inant, in this case gold (Au) nanoparticles. While it is difficult to
demonstrate, it is possible that this lack of studies in the literature re-
flects a bias against publishing negative results. A different study dem-
onstrates that the effect of bisphenol A in immobilization in D. magna
decreases in the presence of PA (polyamide) particles (Rehse et al.,
2018). Teuten et al. (2007) studied the effect of adding “clean” plastic
to a sediment-water system with A. marina contaminated with phenan-
threne (PAH) as a model compound, using an equilibrium partitioning
approach. They concluded that plastic addition would reduce bioavail-
ability to A. marina due to scavenging of phenanthrene by the plastic.
It has been discussed (Koelmans et al., 2013) that MP ingestion may in-
crease bioaccumulation for some chemicals in the mixture (additives,
plasticizers) yet decrease the body burden of these chemicals if they
have opposing concentration gradients between plastic and biota lipids
(Gouin et al., 2011; Koelmans et al., 2013), demonstrating the need of
more studies about on the interactive effects of MPs and other environ-
mental pollutants.
4. Conclusions and future perspectives
The occurrence and accumulation of MPs in the aquatic environ-
ment is nowadays an undeniable fact. It is also undeniable that a
large number of organisms are exposed to these particles and that
this exposure may cause a variety of effects and threaten individuals
of many different species, the ecosystems they live in and, ulti-
mately, humans. The potential deleterious effects of MPs on aquatic
biota have been recognized by the scientific community as demon-
strated by the increasing number of studies in the last years focus-
sing primarily on marine biota. However, the effects of MPs on
freshwater organisms are much less well known.
Overall, results suggest a knowledge gap on the effects of PE MPs on
other organisms beyond fish and PS MPs on all groups of organisms ex-
cept fish and small crustaceans. Polyethylene and PS MPs are clearly the
most studied type of polymers, although others, specifically PP, PES and
PA, may represent a similar danger for aquatic life. Clearly, more re-
search is needed to confirm this issue. While spherical particles are
most commonly used in laboratory studies, fibres and fragments are
the most common types of shapes detected in organisms collected
from field samples and the common size of these particles varies be-
tween 800 and 1600 μm.
Based on the results of this work we point out some issues that need
to be considered, in order to better understand the problematic of MPs
in aquatic systems:
a) Perform more studies of MP effects at environmentally relevant con-
centrations;
b) Study the effects of PP, PES and PA MPs in all groups of animals con-
sidered in this paper since these particles, namely PP, are
manufactured in large scale and detected in aquatic organisms in
the higher quantities than PS;
c) Perform more laboratory studies targeting a range of organism
groups with the most common shapes (fibres and fragments) and
size range (800–1600 μm) of MPs found in biological samples from
the field;
d) Perform more field and laboratory studies with freshwater organ-
isms;
e) Investigate the mechanisms by which MPs affect other groups of or-
ganisms (e.g. echinodermata, cnidaria and porifera) to better deter-
mine the relevance of studies on small crustacea for invertebrates in
general;
f) Understand the mechanisms by which PE affects other groups of or-
ganisms beyond fish and PS MPs on other groups, excepting fish and
small crustaceans;
g) Take into account the interactive effects of MPs and other contami-
nants;
h) Assess the ecotoxicity of MPs in more environmentally relevant con-
ditions, such as multispecies exposures and mesocosms.
i) Encourage the publication of negative results
More investigations are needed in the coming years. They will be
fundamental to understand the mechanism or mechanisms by which
MPs affect aquatic organisms so as to credibly address the real impacts
of these micro-contaminants on the environment.
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.scitotenv.2018.07.207.
Acknowledgments
The authors would like to thank the Swedish Research Council
FORMAS (2017-00029) for funding parts of this study, in the frame of
the collaborative international Consortium (IMPASSE) financed under
the ERA-NET WaterWorks2015 Cofunded Call. This ERA-NET is an inte-
gral part of the 2016 Joint Activities developed by the Water Challenges
for a Changing World Joint Programme Initiative (Water JPI). We are
grateful to Mirco Bundschuh for comments on an earlier version of the
manuscript and to the four anonymous reviewers who provided helpful
guidance in improving the quality of this submission.
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