Journal of Hazardous Materials 417 (2021) 126057

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Journal of Hazardous Materials

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

Microplastics and plankton: Knowledge from laboratory and field studies to

distinguish contamination from pollution
Sabrina M. Rodrigues a, b, *, Michael Elliott c, d, C. Marisa R. Almeida a, Sandra Ramos a
a
CIIMAR - Interdisciplinary Centre of Marine and Environmental Research - Porto University, Porto, Portugal
b
ICBAS – Institute of Biomedical Sciences Abel Salazar - Porto University, Porto, Portugal
c
Department of Biological & Marine Sciences, University of Hull, HU6 7RX, UK
d
International Estuarine & Coastal Specialists Ltd, Leven HU17 5LQ, UK

A R T I C L E I N F O A B S T R A C T

Editor: Dr. Rinklebe Jörg Due to their ubiquitous presence, size and characteristics as ability to adsorb pollutants, microplastics are hy­
pothesized as causing a major impact on smaller organisms, such as plankton. Despite this, there is a need to
Keywords: determine whether these impacts just relate to the environmental presence of the materials or their effects on
Zooplankton biological processes. Therefore, we aimed to 1) review current research on plankton and microplastics; 2)
Phytoplankton
compare field and laboratory experimental findings, and 3) identify knowledge gaps. The systematic review
Ichthyoplankton
showed that 70% of the 147 relevant scientific publications were from laboratory studies and microplastics
Biological effects
Ecological effects interactions with plankton were recorded in 88 taxa. Field study publications were relatively scarce and the
characteristics of microplastics collected in the field were very different from those used in laboratory experi­
ments thereby limiting the comparison between studies. Our systematic review highlighted knowledge gaps in:
1) the number of field studies; 2) the non-comparability between laboratory and field conditions, and 3) the low
diversity of plankton species studied. Furthermore, this review indicated that while there are many studies on
contamination by microplastics, the effects of this contamination (i.e., pollution per se) have been less well-
studied, especially in the field at population, community, and ecosystem levels.

1. Introduction
The worldwide mass production of plastic has been increasing
annually due to its versatile nature, its durability, lightness and wide
use, reaching a total of 368 Mt in 2019 (PlasticEurope, 2020). Many
plastic products are single-use and, without an environmentally bene­
ficial means of disposal, recycling or re-use, will eventually contaminate
all environments. Plastics, including microplastics (MPs, particles <5
mm), occur in all aquatic habitats, such as ocean, rivers, lakes, and es­
tuaries, creating a global problem (Li et al., 2018; Jacob et al., 2020;
Maryani et al., 2020). Microplastics can be categorized as primary or
secondary depending on their origin: primary microplastics are indus­
trially produced as smaller particles, whereas secondary microplastics
result from larger plastic formations that fragment into progressively
smaller particles and debris due to UV radiation, abrasion or biodegra­
dation (Castillo et al., 2016). There has been an increasing scientific and
societal concern about micro- and macro-plastics in the environment,
given their potential to negatively affect many species. This ultimately
has led to their specific inclusion in the indicators and targets of the UN
Sustainable Development Goal (SDG) 14 – ‘Conserve and sustainably use
the ocean, seas and marine resources for sustainable development’: in
which Target 14.1 specifically refers to plastics pollution (Cormier and
Elliott, 2017).
The impacts of plastics on megafauna such as important commercial
fish species, mammals and invertebrates have been well documented (e.
g., Puskic et al., 2020; Zantis et al., 2020). However, smaller organisms,
such as plankton, are likely to be increasingly affected as the introduced
and degraded MPsc particle sizes coincide with their prey size
(zooplankton and ichthyoplankton) or their ability to entrain particles
(phytoplankton). Coupled with the predominantly filter-feeding mech­
anisms of many zooplankton, this interaction is of increasing concern
given the position of such organisms at the base of marine food webs
with a dominant role in ecosystem functioning, including biogeochem­
ical, nutrient and carbon cycling (Galloway et al., 2017; Botterell et al.,

* Correspondence to: CIIMAR - Interdisciplinary Centre of Marine and Environmental Research - Porto University, Terminal de Cruzeiros Do Porto de Leixões,
Avenida General Norton de Matos, S/N, 4450-208, Matosinhos, Portugal.
E-mail address: smagalhaes@ciimar.up.pt (S.M. Rodrigues).

https://doi.org/10.1016/j.jhazmat.2021.126057
Received 19 December 2020; Received in revised form 30 April 2021; Accepted 4 May 2021
Available online 8 May 2021
0304-3894/© 2021 Elsevier B.V. All rights reserved.
S.M. Rodrigues et al. Journal of Hazardous Materials 417 (2021) 126057

2019). Furthermore, their position in the food chain and their small size
makes these planktonic stages sensitive and vulnerable to environmental
threats (Ramos et al., 2015; Botterell et al., 2019). Thus, it is important
to investigate the impacts that this new class of contaminants poses to
plankton and if MPs compromise the plankton diversity, ecological
functions and food chains (e.g., Botterell et al., 2019; Franzellitti et al.,
2019).
Here we distinguished between contamination, as the presence of a
human-derived material in the environment, and pollution per se, as the
biological effect of those contaminants which will reduce the fitness for
survival of one or more levels of biological organization from the cell to
the ecosystem (Borja and Elliott, 2019; Souza et al., 2020). We
emphasize this distinction given the Latin root of contamination
meaning to make impure, i.e., the addition of materials in type or
quantity not normally present in the environment but in which a bio­
logical impact is not assumed. The current review aims to test the earlier
suggestion that for plastics there are more studies on contamination than
on pollution per se (Borja and Elliott, 2019).
The current study aimed to systematically review the scientific
literature regarding plankton and MPs interactions, comparing field and
laboratory research, in particular in terms of: i) MPs characteristics; ii)
methodologies; iii) plankton groups studied; iv) biological, ecological,
and ecosystem effects of MPs on plankton, and v) knowledge gaps.

2. Methods
Fig. 1. Flowchart of the stages of identification of publications used in the
systematic review.
2.1. Search strategy

The literature search was carried out using the main scientific liter­
Table 1
ature databases, namely Scopus®, Science Direct®, and Web of Sci­ Data variables and corresponding categories used to extract data from the
ence®. A sensitive systematic search strategy that used the search string publications included in the systematic review regarding plankton and micro­
"(microplastic OR "plastic particles" OR fiber OR "plastic fibers") AND plastics interactions.
(plankton OR ichthyoplankton OR zooplankton OR "fish larvae" OR
Data variables Categories
phytoplankton)” on article title, abstract and keywords was applied. The
Type of publication e.g., methodology, results, modeling
search included all the articles published and registered on the databases
Condition laboratory, field
until the cut-off date of 1 March 2020, hence data for 2020 will be Plankton group e.g., phytoplankton, zooplankton, ichthyoplankton
incomplete. Field studies:
Environment e.g., sea, bay, estuary, lake, river, channel
2.2. Literature selection criteria and review process Country of sampling e.g., Argentina, France, China, Brazil
Assessed e.g., water, ingestion
Methodology e.g., plankton net, bucket; neuston net, bongo net,
Several selection criteria were established regarding which publi­ MP morphology e.g., fibers, fragments
cations to include in this review, namely that they: 1) included at least MP concentration e.g., MPs m-3, MPs mL-1
one species of plankton, 2) were written in English, and 3) excluded Polymer confirmation e.g., FTIRa, Raman
Lab-base studies:
reviews, opinion papers, book chapters and conference papers. No
Assessed e.g., ability to ingest, effects of ingestion
country or date restrictions were included in the search in order to Experiment conditions e.g., no food, with food, starvation period
collect all the available information. The systematic review process MP morphology e.g., beads, particles, fibers, powder; secondary MPs
followed the following steps: firstly, a total of 1 457 papers were iden­ Polymer e.g., PE, PA, PET, PSb
tified as potentially relevant. References in relevant reviews were MPs ingestion yes, no
MPs effects e.g., growth, survival, reproduction, feeding
screened for additional publications and 22 additional potentially rele­
a
vant publications were identified. Secondly, the titles and abstracts of all FTIR (Fourier-transform infrared spectroscopy).
b
publications were screened that resulted in the rejection of 1 190 pub­ PE (polyethylene), PA (polyamide), PET (polyethylene terephthalate) and PS
lications which did not meet our criteria. Additionally, all the duplicated (polyester).
entries were removed. Thirdly, the full text of the remaining 155 pub­
lications was then retrieved, and a further selection process was un­ Descriptive statistics were used to calculate the number of publica­
dertaken, and 8 publications were considered not eligible or relevant for tions relating to laboratory or field studies and regarding experimental
our review. This gave 147 publications considered suitable for use in the conditions, such as MPs type and polymer, food availability, plankton
review (Fig. 1). group studied. To compare with field publications, information
regarding MPs concentration, and characteristics was collated through
2.3. Data collection and analysis tables, as were the species identified in the publications. Moreover, we
investigated whether the effects varied according to plankton groups,
The extracted data from the systematic review included the type and MPs concentration, food availability, and environment (laboratory or
aim of publication, group of plankton studied, the descriptions of the field conditions). Finally, we mapped the geographical distribution of
study site in field studies (country and type of environment), method­ field publications analyzed. Although the color of the MPs was found to
ology and/or experimental conditions, MPs characteristics (concentra­ be important in clear freshwater in experimental conditions (Xiong
tion, polymer, type/shape), main results, and conclusions. The et al., 2019), this information was not consistently given in marine
component publications were analyzed descriptively (Table 1). studies and so not included here.

2
S.M. Rodrigues et al. Journal of Hazardous Materials 417 (2021) 126057

3. Results and discussion
3.1. Main results
While the number of studies related to MPs has increased greatly in
recent decades (Borja and Elliott, 2019), considerably fewer publica­
tions have focused on the relationship between MPs and plankton or­
ganisms. It is of note that many studies, for example, those that collected
water samples using plankton nets, only aimed to investigate MPs
contamination (MPs concentration in water) and did not include in­
teractions with the plankton. Hence, the number of studies that met our
criteria and focused both on MP and, at least, one group of plankton was
relatively low, thus reinforcing the suggestion that publications focus­
sing on the relationship between MP and plankton are not common.
Applying the above selection criteria led to the selection of a total of 147
publications (Table S1 – supplementary material). These include 5 on
methods (three of them also presenting results) (e.g., Sun et al., 2017;
Beiras et al., 2019b), 2 on modelling (Troost et al., 2018; Kong and
Koelmans, 2019), and 143 giving empirical research (e.g., Cong et al.,
2019; Cunha et al., 2019; Alfonso et al., 2020) (Fig. 2). It is of note that
approx. 86% of the publications included in this review were published
after 2015 (Fig. S1.a - Supplementary material), showing an increase of
interest in MPs and planktonic interaction in recent years. This trend is
likely to continue given the growing public awareness and scientific
interest in MPs pollution worldwide (Borja and Elliott, 2019). It is
acknowledged that while the search may have missed some more inac­
cessible publications, it does contain a cross-section of the
peer-reviewed research thereby allowing valid conclusions.
Many of the publications included in this review analyzed both the
ability of plankton to ingest MPs and their effects, with special attention
on individual and biological effects (e.g., Cole et al., 2019; Coppock
et al., 2019; Li et al., 2020a). A few publications (8%) evaluated the
wider ecological effects of MPs on plankton such as Elizalde-Velázquez
et al. (2020) that investigated the possible translocation and trophic
transfer of MPs or Troost et al. (2018) that question whether MPs affect
the marine ecosystem productivity. From the 147 publications selected,
less than 50 publications (<1/3) resulted from field studies (Fig. 2), with
most focusing on contamination (e.g., Rodrigues et al., 2019; Alfonso
et al., 2020). In turn, a similar small proportion of these field studies
(30%) assessed the biological effects of MPs on the plankton structure
and functioning at various levels of biological organization, including
population and community changes (i.e., pollution per se) (e.g., Kang
et al., 2015; Katija et al., 2017). These findings indicate the prevalence
of publications which describe contamination rather than pollution,
despite the titles of some publications describing the contamination
(presence of MPs) as ‘pollution’ (thereby assuming biological effects).
This misinterpretation has been common for many materials in the field
of marine pollution in which earlier studies measure the presence of
contaminants but the later studies measure the consequences of that
contamination as pollution (e.g., Borja and Elliott, 2019; Sheppard et al.,
2021).
Regarding the groups of plankton studied, 67% of publications
included in the review (Fig. 2) analyzed zooplankton species (e.g.,
Dapnhia magna, Aljaibachi and Callaghan, 2018; Gammarus fossarum,
Blarer and Burkhardt-Holm, 2016) compared to 32% on phytoplankton
(e.g., Tetraselmis chuii, Davarpanah and Guilhermino, 2015; Chlamydo­
monas reinhardtii, Li et al., 2020a) and ichthyoplankton species (e.g.,
Oryzias melastigma, Cong et al., 2019; Danio renio, Karami et al., 2017).
From the publications selected, a total of 88 taxa were used as
case-studies, with a dominance of Dapnhia magna, a freshwater species.
3.2. Comparability between field and laboratory studies
3.2.1. Field studies
The ubiquitous presence of MPs in aquatic environments is of
particular concern since they represent an increasing threat to marine
organisms and ecosystems. Thus, the monitoring of contamination (as
the presence of MPs) in these environments is essential as a first step
towards determining biological effects. From the 45 field studies pub­
lications included in this review, two-thirds (70%) related to the open
sea, with fewer studies focused on estuaries (n = 6, e.g., Lima et al.,
2014; Rodrigues et al., 2019), rivers (n = 3, e.g., Moore et al., 2002;
Payton et al.,2020), bays (n = 2, Collignon et al., 2014; Figueiredo and
Vianna, 2018), and channels (n = 1, Steer et al., 2017) (Fig. 3, Table 2).
Furthermore, more than half of the field studies included in this review
were performed in Europe (n = 18, e.g., Steer et al., 2017; Rodrigues
et al., 2019) and Asia (n = 12, e.g., Sun et al., 2017; Amin et al., 2020)
(Fig. S1.b – Supplementary material), showing that information on MPs
and plankton interaction is still limited in most aquatic environments
worldwide.
Most of the plethora of field study publications (n = 45) focused on
contamination (as the presence of MPs) (n = 30), only 7 studies inves­
tigated the biological effects in the plankton structure and functioning (i.
e., pollution per se) and 8 studies investigated both (Table 2). MPs
contamination reported in those publications showed a wide range of
values, from less contaminated areas such as a coastal area in Brazil
(0.000093 MPs m− 3, Lima et al., 2019) or a river in South Carolina
(0.0015 MPs m− 3, Payton et al., 2020) to highly contaminated

Fig. 2. Distribution of publications regarding microplastics and plankton interactions according to type of publication, condition of study, and plankton group
studied (NB, the term ‘plankton’ denotes those studies which did not separate the organisms into different groups of plankton).

3
S.M. Rodrigues et al.
Fig. 3. Distribution of field studies publications regarding microplastic and plankton interaction according to the environment sampled, what was assessed and, in
the case of evaluation of ingestion, if this was analyzed only the stomach or the whole organism.
environments such as the Mediterranean Sea (44 * 1016 MPs m− 3,
Pedrotti et al., 2016) or the North Pacific (19 * 1016 MPs m− 3, Moore
et al., 2001) (Table 2). Studies on freshwaters reported low values of
contamination between 0.0015 MPs m-3 (South Carolina, Payton et al.,
2020), 0.32 MPs m-3 (Austria, Lechner et al., 2014) and 8 MPs m-3
(California, Moore et al., 2002) and MPs were mostly fragments, pellets,
flakes and spherules. A similar scenario was observed in studies on
estuarine waters, with MPs concentrations ranzing between 0.048 MPs
m-3 (Brazil, Lima et al., 2016b), 0.17 MPs m-3 (Portugal, Rodrigues et al.,
2019) and 0.26 MPs m-3 (Brazil, Lima et al., 2014, 2015) except for two
studies that observed higher levels of MPs contamination, namely in
Argentina (139 MPs m-3, Pazos et al., 2018) and in Australia (23-1892
MPs m-3, Hitchcock and Mitrovic, 2019). Most of the field studies
included here investigated MPs contamination in seawater and showed a
wider range of MPs contamination values, from 0.000093 MPs m-3 in
Brazil (Lima et al., 2016a) to 19 * 1016 MPs m-3 in Portugal and Spain
(Herrera et al., 2020) and 44 * 1016 MPs m-3 in the Mediterranean Sea
(Pedrotti et al., 2016). Furthermore, some studies found a wide vari­
ability of MPs contamination; for example, Hitchcock and Mitrovic
(2019) observed between 23 and 1892 MPs m− 3 in an Australian estu­
ary, and Gorokhova (2015) observed between 102 and 104 MPs m− 3 in
the Baltic Sea. Different environments had similar levels of contamina­
tion (Table 2) indicating comparable threats to the wildlife from MPs in
these ecologically biodiverse and important environments.
Several studies focused on zooplankton and MPs contamination in
water, reporting a ratio of 0.13 MP ind-1 (copepods) (Sun et al., 2018a)
or 1.17 MP ind-1 (stomapods) (Sun et al., 2018b), while other studies
focused on ichthyoplankton and observed a ratio of 1.5 MP ind-1
(Rodrigues et al., 2019) or between 1 and 27 MP ind-1 (Steer et al.,
2017). The proportion of publications from field analysis was very small,
however, information regarding MP ingestion and biological effects on
plankton was even scarcer. Of studies determining MP ingestion
(n = 14), 6 of them analyzed only the stomach of the organisms (e.g.,
Steer et al., 2017; Prata et al., 2018) compared to 8 in which whole
organism was digested (e.g., Sun et al., 2017; Kim et al., 2017) (Fig. 3);
some analyzed zooplankton taxa (such as Desforges et al., 2015 and
Brandon et al., 2020) while others analyzed ichthyoplankton (such as
Steer et al., 2017) (Table 2). Sun et al. (2018a, 2018b) investigated MPs
ingestion in zooplankton taxa such as Amphipoda, Chaetognatha and
Euphausiacea and reported an average ingestion level between 0.13 and
0.35 MPs ind-1, mostly of fibers, while Zheng et al. (2020) investigated
zooplankton and ichthyoplankton taxa, namely Chaetognatha, fish
larvae, Medusae and Amphipoda and reported an ingestion level be­
tween 0.01 and 0.12 MPs ind-1 with a predominance of fibers and
fragments (Table 2). Furthermore, Zheng et al. (2020) observed that
4
Journal of Hazardous Materials 417 (2021) 126057
Medusae followed by fish larvae were the two taxa with the highest
levels of ingestion (0.056–0.117 MP ind-1 and 0.097 MP ind-1, respec­
tively) while Kosore et al. (2018) reported that Chaetognatha had the
highest values of ingestion (0.46 MP ind-1).
Publications included in this review reporting aquatic field studies
described a large variety of MP types, shapes and polymers (Table 2).
Half of the publications (n = 24) reported fibers (e.g., Aytan et al., 2016;
Sun et al., 2017) and fragments (e.g., Ory et al., 2017; Amin et al., 2020)
as the most common types of MP collected in water or ingested. Paint
particles, styrofoam (Kang et al., 2015), filaments (Kosore et al., 2018)
and spherules (Lechner et al., 2014) were also reported in water samples
(Table 2). A few publications (n = 5) categorized MPs as hard and soft
particles (e.g., Rodrigues et al., 2019; Lima et al., 2016a) whereas 9
publications gave no information regarding the type of MPs collected (e.
g., Lattin et al., 2004; Panti et al., 2015). Twenty-two studies performed
polymer confirmation with specific analysis such as FTIR or Raman, and
polyethylene was one of the most commonly plastic polymers observed
in field environmental studies (n = 13) (e.g., De Lucia et al., 2018; Ory
et al., 2017). Polypropylene (n = 5, e.g., Kosore et al., 2018), polyester
(n = 5, e.g., Collignon et al., 2012) and polyamide (n = 4, e.g., Amin
et al., 2020) were also observed in these studies, as well as other poly­
mers such as rayon, cellophane and nylon (e.g., Zheng et al., 2020)
(Table 2). One of these publications only confirmed that the particles
were plastic, but did not give further information (Kang et al., 2015).
Plankton nets were one of the most common equipment’s used to
collect water samples since they capture the same size range of MPs that
directly affect the smaller organisms. Forty-two publications specified
the sampling technique, and the plankton net was the most used
(n = 33), including bongo net (n = 8, e.g., Brandon et al., 2020), epi­
neuston net (n = 1, Ory et al., 2017), neuston net (n = 5, e.g., Yeo et al.,
2020) and norpac net (n = 1, Amin et al., 2020) (Fig. 5). Moreover,
various mesh sizes were used - including 500 µm (e.g., Lima et al., 2014;
2015), 300 µm (e.g., do Sul et al., 2013; Lima et al., 2016a), and 200 µm
(e.g., Fossi et al., 2012; Aytan et al., 2016). The equipment manta net
(n = 9, e.g., Moore et al., 2002), bucket (n = 4, e.g., Alfonso et al.,
2020), and stationary conical driftnets (n = 1, Lechner et al., 2014) were
also used. From the total number of studies here included, there were
relatively few field studies that investigated MPs contamination in water
and reported both high and low values of MP contamination and used
various methods to collect MPs (Table 2). For example, from the six
studies that investigated MP contamination in estuarine waters, samples
were collected with a plankton net (23–1892 MPs m− 3, Hitchcock and
Mitrovic, 2019) or a bucket (139 MPs m− 3, Pazos et al.,2018) (Table 2),
and both methods resulted in high concentrations of MPs observed. In
seawater, not only bongo nets (8.3 * 106 MPs m− 3, Brandon et al.,
S.M. Rodrigues et al. Journal of Hazardous Materials 417 (2021) 126057

Table 2
Summary of field studies reporting MPs and plankton interactions separated between contamination (MPs concentration on water) and pollution (MPs ingested)
studies.
Environment Sampling Plankton group MPs MP morphology Polymer Publication
location concentration

Contamination (MPs Lake Argentina Zooplankton1 140–180 MPs Fibers PEa Alfonso et al., 2020
on water) m− 3
Channel England Ichthyoplankton7 0.26 – 3.79 MPs Fibers Nylon, PA-PP, Steer et al., 2017
m− 3 rayon
8
River Austria Ichthyoplankton 0.32 MPs m− 3 Pellets, flakes, – Lechner et al.,
spherules 2014
4 − 3
California Zooplankton 8 MPs m Fragments – Moore et al., 2002
South Carolina Zooplankton1 0.0015 MPs Fragments – Payton et al., 2020
m− 3*
Estuary Australia Zooplankton7 23–1892 MPs Fragments – Hitchcock and
m− 3 Mitrovic, 2019
Argentina Zooplankton; 139 MPs m− 3 Fibers – Pazos et al., 2018
Phytoplankton1
− 3
Brazil Zooplankton; 0.26 MPs m – – Lima et al., 2015
Ichthyoplankton7
3
Zooplankton; 0.26 MPs m− Hard, soft particles – Lima et al., 2014
Ichthyoplankton7
Ichthyoplankton7 0.048 MPs m− 3 Hard particles – Lima et al., 2016b
Portugal Ichthyoplankton7 0.17 MPs m− 3 Hard particles – Rodrigues et al.,
2019
3
Bay Brazil Zooplankton, 4.8 – 11 MPs m− Fragments PEa Figueiredo and
Ichthyoplankton7 Vianna, 2018
Mediterranean Zooplankton4 0.0154 MPs m− 3
Filaments, films PSa Collignon et al.,
Sea 2014
Sea Black Sea Zooplankton7 600–1200 MPs Fibers – Aytan et al., 2016
m− 3
7
Baltic Sea Zooplankton 102 104 m− 3 – – Gorokhova, 2015
Brazil Zooplankton7 0.01 MPs m− 3 Secondary MPs – do Sul et al., 2013
Ichthyoplankton7 0.000093 MPs Hard particles – Lima et al., 2016a
m− 3
3
China Zooplankton; 0.0033 MPs m− Fibers PAa Amin et al., 2020
Ichthyoplankton5
Zooplankton2 0.13 MPs m − 3
Fragments PE, PP a
Sun et al., 2018a,
2018b
a
Zooplankton, 0.41–2.03 MPs Fibers Cellophane, PET Zheng et al., 2020
Ichthyoplankton2 m− 3
California Zooplankton4 3.92 MPs m− 3 – – Lattin et al., 2004
Greenland Zooplankton7 0.99–2.38 MPs Filaments PE, PSa Amélineau et al.,
m− 3 2016
Italy Plankton7 0.3 MPs m− 3 Fibers PEa De Lucia et al.,
2018
Korea Zooplankton4 1.9–5.5 MPs m− 3
Hard plastic, paint, – Kang et al., 2015
fiber, styrofoam
3
Kenya Zooplankton, 110 MPs m− Filaments PPa Kosore et al., 2018
Ichthyoplankton1, 7

Mediterranean Plankton4 44 * 1016 MPs – PE, PP, PAa Pedrotti et al.,

Sea m− 3 * 2016
4
Plankton 4.3 * 1016 MPs Fragments – Faure et al., 2015
m− 3 *
Zooplankton4 0.0395 MPs m− 3 Filaments, films PSa Collignon et al.,
* 2012
Zooplankton7 0.17 MPs m− 3 – – Panti et al., 2015
Zooplankton6,7 9.6 MPs m− 3 – – Fossi et al., 2012
Mexico Zooplankton2.6 5 – 18 MPs m− 3 Irregular particles, – Di Mauro et al.,
fibers 2017
North Pacific Zooplankton2 8.3 × 106 MPs Fibers, fragments – Brandon et al.,
m− 3 * 2020
Zooplankton4 19 * 1016 MPs Thin films – Moore et al., 2001
m− 3 *
Norway Zooplankton4 0.34 MPs m− 3 Fibers PE, PS, PAa Lusher et al., 2015
Portugal Zooplankton6. 7
0.002–0.04 MPs – PEa Frias et al., 2014
m− 3
Portugal, Spain Zooplankton2,4 1914 MPs m− 3 * Fibers, fragments – Herrera et al., 2020
South Pacific Zooplankton3 0.06 MPs m− 3 Fragments PEa Ory et al., 2017
Pollution (MPs Channel England Ichthyoplankton – Fibers Nylon, PA-PP, Steer et al., 2017
ingestion) rayon
River South Carolina Zooplankton – Fragments, fibers – Payton et al., 2020
Sea China Zooplankton 0.07–1.17 MPs Fibers Organic oxidation Sun et al., 2018a,
ind-1 polymers 2018b
Zooplankton 0.13–0.35 MPs Fibers PSa Sun et al., 2018a,
ind-1 2018b
Zooplankton 0.52 MPs ind-1 Fibers PETa Zhang et al., 2019
(continued on next page)

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S.M. Rodrigues et al. Journal of Hazardous Materials 417 (2021) 126057

Table 2 (continued )
Environment Sampling Plankton group MPs MP morphology Polymer Publication
location concentration
1
Zooplankton; 1 MPs ind− Fragments PAa Amin et al., 2020
Ichthyoplankton
Zooplankton; 0.01–0.12 MPs Fibers, fragments Cellophane, PETa Zheng et al., 2020
Ichthyoplankton ind-1
a
KenyBucketa Zooplankton, 0.16–0.46 MPs Filaments PE Kosore et al., 2018
Ichthyoplankton ind-1
Mediterranean Ichthyoplankton – Fibers – Uriarte et al., 2019
Sea
North Pacific Zooplankton 1–160 MPs ind-1 Fibers, fragments – Brandon et al.,
2020
Zooplankton 0.026–0.058 MPs Fibers PE, resin, Desforges et al.,
ind-1 cellophanea 2015

Methodology used to collect water samples: 1Bucket, 2Bongo net, 3Epineuston net, 4Manta net, 5Norpac net, 6Neuston net, 7Plankton net, 8stationary conical driftnets -
Methodology used to collect water samples.
*MPs concentration was converted to MPs m− 3 for comparison.
a
PE (polyethylene), PA (polyamide), PET (polyethylene terephthalate), PS (polyester) and PP (polypropylene).

2020), as well as manta nets (19 * 1016 MPs m− 3, Moore et al., 2001 and
19 * 1016 MPs m− 3, Pedrotti et al., 2016) (Table 2) observed high MPs
concentrations. It is important to note that these comparisons must be
tempered by differences in sampling methodologies, and are only
intended to show that, independently of the MPs concentration,
plankton nets were one of the most common methods for monitoring
plastic debris in the aquatic environment, sampling large volumes of
water and capturing the size range of MPs that directly affect the smaller
marine organisms. We acknowledge that subtle differences in sampling
methods will affect the results but that in metanalysis studies such as this
it is not possible to restrict the interrogation to only those few studies
with identical methods. Furthermore, including papers with differing
techniques will still indicate the main phenomena being investigated.
3.2.2. Laboratory-based studies
From the total of 103 laboratory-based studies, 94 focused on the
ability of an organism to ingest MPs (e.g., Cole et al., 2013; Vroom et al.,
2017) and/or the effects of ingestion/exposure to MPs (e.g., Aljaibachi
and Callaghan, 2018; Au et al., 2015). Nine publications, classified as
others, focused on changes in faecal pellets (Cole et al., 2016), aggre­
gation (Long et al., 2015, 2017; Möhlenkamp et al., 2018; Cunha et al.,
2019), ability to reduce MPs size (Dawson et al., 2018), ability to
degrade MPs (Hodgson et al., 2018), effects on marine productivity
(Troost et al., 2018) and effects on the ecosystem (Kong and Koelmans,
2019). Hence, laboratory-based studies focused mostly on MPs ingestion
by zooplankton (45%), including eggs and fish larvae (i.e.,
ichthyoplankton) and MPs effects on plankton (47%), and only a small
fraction (8%) studied other interactions of MPs and plankton.
To allow the extrapolation of laboratory-based results to the envi­
ronment, it is necessary that laboratory conditions mirror field condi­
tions. In addition, the methodologies and experimental conditions can
simulate other environmental conditions and predict future scenarios,
such as impacts from severely contaminated areas or climate changes.
However, the review showed that many laboratory-based studies fol­
lowed a similar trend and experimental conditions, which on the one
hand improves the comparability among experiments but on the other
hand are not representative of what has been found on field. For
example, almost half of the laboratory-based studies were performed
using polystyrene (PS) (n = 49, e.g., Aljaibachi and Callaghan, 2018;
Cole et al., 2015) and polyethylene (PE) (n = 25, e.g., Beiras et al., 2018;
Felten et al., 2020), while field studies reported a greater variety of
polymers (e.g., polyamide, polypropylene, rayon, nylon, cellophane).
Exceptionally, polyvinyl chloride (PVC) (n = 7, e.g., Schrank et al.,
2019), polyamide (PA) (n = 4, Rehse et al., 2018), polyethylene tere­
phthalate (PET) (n = 3, e.g., Heindler et al., 2017) and polypropylene
(PP) (n = 3, e.g., Wu et al., 2019) were rarely used in laboratory-based
studies (Fig. 4). Regarding the shape, most studies focused on spherical
MPs (beads) (n = 50), probably because this is the most common and
easily obtained commercial shape; however, that was not the most
commonly observed shapes in field studies which were fibers and frag­
ments. In contrast, only 25% of the publications recorded other MPs
shapes, such as fibers (n = 7, e.g., Jemec et al., 2016) and only 11

Fig. 4. Distribution of laboratory-based publications regarding microplastics and plankton interaction according to the characteristics of MPs, namely polymer,
shape, and type, used in laboratory experiments.

6
S.M. Rodrigues et al.
publications recorded irregular particles or secondary MPs (e.g., Cop­
pock et al., 2019; Pannetier et al., 2020) (Fig. 4). Again, these features
indicate that the experimental conditions differ from those in the field.
The concentration and exposure times of MPs used during experi­
ments also highly varied, thus increasing the difficulty of comparisons
between studies. Most studies used several concentrations to assess the
dose-response curve, from a few to hundreds of particles per unit vol­
ume, e.g., 5, 50, and 250 MPs mL-1 (Setälä et al., 2016), to 50–200 MPs
mL-1 (Vroom et al., 2017). It is of note that several studies predicted the
effects of MPs in environments with low food availability and high MPs
concentration using thousands of MPs per unit volume, e.g., 10 000
particles 104 particles MPs mL-1 (Setälä et al., 2014) to 500–60000 MPs
mL-1 (Blarer and Burkhardt-Holm, 2016) or even 102–105 MPs mL-1
(Bosker et al., 2019). Other studies used only one MPs concentration (e.
g., Ayukai, 1987), concentrations similar to those found in less
contaminated areas (e.g., Lönnstedt and Eklöv, 2016), or even a ratio of
microplastic to algal cells (Bosker et al., 2019). Unfortunately, nine of
the studies did not indicate the MPs characteristics or concentration
used, or the MPs concentration was expressed in quantities that do not
allow valid comparisons between studies.
Several laboratory studies showed previously that the experimental
conditions, such as a period of starvation prior to the experiment, can
affect the result obtained (e.g., Ayukai et al., 1987). The systematic re­
view revealed that of the 25 studies that investigated the ability of or­
ganisms to ingest MP, some included a starvation period (n = 4) lasting
from few hours (e.g., 3 h, Ayukai, 1987 or 4 h, Vroom et al., 2017), to
12 h (e.g., Cong et al., 2019) or even 48 h (e.g., Blarer and
Burkhardt-Holm, 2016). This depuration step is used to effect gut
clearance, enhance hunger, and ensure a comparable stage of hunger
among the organisms. However, this may be criticized as creating a
non-normal condition despite standardizing the organism state; for
example, Ayukai (1987) showed that starved organisms tended to ingest
more plastic particles than well-fed organisms, thereby influencing the
results. Importantly, Jemec et al. (2016) showed that organisms fed
before the experiment with MPs showed no effects on mortality whereas
increased mortality occurred in those organisms not pre-fed prior to the
experiment.
In addition to the above-mentioned influences on the study results,
another important condition variable is whether or not other sources of
food were used during the experiment with MPs. From the 25 laboratory
studies that investigated ingestion, 17 involved feeding the organisms
during the experiment (e.g., Blarer and Burkhardt-Holm, 2016; Bosker
et al., 2019) whereas six studies gave only MPs to the organisms (e.g.,
Chen et al., 2020; Frydkjær et al., 2017). Three studies showed that
when a mixture of MPs and food was offered, organisms tend to ingest
significantly more food and that MPs only represent a significant part of
the diet of the organism when MPs strongly dominate the food available
(Huntley et al., 1983; Fernández et al., 2004; Aljaibachi and Callaghan,
2018). Cheng et al. (2020) recently suggested that low food availability
may increase the ingestion and retention of MPs in organisms by
enhancing the encounter rates. Only Vroom et al. (2017) employed a
starvation period and no source of food during the experiments. Hence,
experimental conditions in which the organismal natural feeding re­
gimes were altered may not necessarily reflect conditions in the natural
state. For example, Štrus et al. (1985) and Nelson (2011) showed that
some organisms exhibit a highly selective feeding behaviour and factors
such as starvation can mask these abilities and induce them to feed
unselectively.
3.3. Dissimilarity and non-comparability between laboratory and field
conditions
To evaluate the potential impacts of MPs on planktonic organisms, a
number of laboratory experiments have been performed over recent
years. However, the systematic review showed that most laboratory
studies tended not to reflect the level of contamination encountered in
7
Journal of Hazardous Materials 417 (2021) 126057
most ambient conditions. This is a common problem in toxicological
studies which aim to obtain a dose-effect response irrespective of con­
ditions found in the environment (Rand, 1995). Hence, the results and
effects observed in these studies should be treated with caution and
researchers must include standardized measures of the concentration
used.
Most studies on the bioavailability and effects of microplastic used
PS and PE spherical particles, while fewer data are available for fibers,
fragments, and other polymers most commonly found in aquatic envi­
ronments. In fact, the MPs characteristics found in aquatic environments
or ingested by zooplankton and ichthyoplankton (Table 2) showed a
great variability either in shape, or even in polymer, from fragments,
fibers, films, paint chips and foam; however, some of these types were
rarely used in experiments. In contrast, the most common types used in
laboratory experiments, such as spherules or pellets, were exceptionally
reported in field studies (Table 2). The dissimilarity in MPs character­
istics between laboratory studies and field samples therefore hindered
the extrapolation of the effects observed in the laboratory to aquatic
environments. For example, fiber was the most common MP type re­
ported in field studies investigating ingestion (Table 2), whereas only 7
laboratory-based studies used this type of MP (e.g., Blarer and
Burkhardt-Holm, 2016; Zocchi and Sommaruga, 2019). In fact, Cole
et al. (2019) emphasized that shape could influence microplastic
bioavailability since PA fibers (using environmentally relevant MP
concentrations) produced significantly negative effects (such as on prey
selectivity, feeding rate and premature molting) compared to PA beads
that showed non-significant negative effects. Similarly, Lagarde et al.
(2016) showed that different polymers (in high concentrations) had
different effects (e.g., on hetero-aggregation) when interacting with
phytoplankton. This dissimilarity in MP characteristics emphasizes the
need for more laboratory-based studies that use MP with the same
characteristics as those found in the environment to understand the
actual ecological impacts of this new contaminant.
One of the main limitations of laboratory studies was that the ex­
periments usually used virgin MPs, which had not been ‘weathered’, i.e.,
exposed to environmental conditions which otherwise would have
affected their surface properties and coatings by diatoms, bacteria, and
fungi such as yeasts (Flemming et al., 2010); this is important as the
biofilm would have increased the palatability of the MPs. For example,
Vroom et al. (2017) showed that MPs (in realistic environmental con­
centrations) previously exposed to marine conditions were ingested at
higher rates than primary MPs, and suggested that this preference could
be related to the formation of a biofilm. Moreover, Pannetier et al.
(2019), using environmentally-weathered MPs (i.e., only using MPs
collected from aquatic environments) in concentrations between 70 and
7000 MPs L− 1, showed that the exposure to pollutants adsorbed to the
surface of those MPs can cause death, decreased body ratios, DNA
breaks, and alterations in swimming behavior. They also showed that
the toxicity of MPs varied from one sample to another, depending on
polymer composition, weathering and contaminant content, high­
lighting the importance of performing laboratory-based studies in con­
ditions similar to those found in aquatic environments. All of these
studies emphasize that the shape and polymer type can influence greatly
the impact and toxicity to the organisms, thus showing the importance
of using different types, polymers, and even MPs previously collected
from aquatic environments in laboratory studies. Many of the laboratory
experiments had similar conditions, which improved the comparability
among experiments. However, if these conditions were not similar to
those found in natural aquatic environments, extrapolating from one to
another would not be possible and, ultimately, does not represent the
environmental hazard to which organisms are exposed. This is particu­
larly important as the most common MP types found in the environment
(secondary MPs, fragments, fibers) can have a greater capacity to
negatively affect wildlife than spherical MPs due to their roughness and
irregularity (e.g., Ogonowski et al., 2016; Ziajahromi et al., 2017; Cole
et al., 2019). In particular, some of the experiments with beads and
S.M. Rodrigues et al.
spherules showed a high rate of egestion and reported no effects, in
contrast to irregular particles that due to their characteristics tend to be
entangled, cause physical injuries, and consequently have a greater ca­
pacity to cause negative biological effects.
As indicated above, MPs concentrations used in laboratory studies
and experimental conditions (often with starvation periods and low food
availability) do not simulate natural aquatic environmental conditions.
Some of these studies aimed to obtain a dose-effect response irrespective
of both the conditions found in the environment and the concentration
used. In that case, the effects observed are unlikely to occur in envi­
ronments with low levels of contamination. As such, it is not valid to
extrapolate from laboratory to field effects and comparisons must be
made with caution. Some of the most severe effects reported in labora­
tory studies, such as impaired development or death (e.g., Pacheco et al.,
2018; Bosker et al., 2019) were obtained using non-realistic concen­
trations (e.g. 105 MPs L-1). Since the environmental effects are very
challenging to assess, it is difficult to determine whether the effects re­
ported in laboratory experiments can occur in the environment. Most of
the field studies included in this review reported a degree of MPs
contamination (< 10–102 particles m-3) lower than those used in labo­
ratory experiments, that frequently reached 106 and even 109 MPs m-3
(Table S2 – Supplementary material). Hence, effects observed with these
MPs laboratory concentrations cannot validly be extrapolated to the
environmental consequences, thereby questioning what type of effects
occur in organisms in aquatic environments.
3.4. Plankton groups studied
Of the selected 147 studies, 64% focused only on zooplankton
(n = 94, e.g., Costa et al., 2020) whereas 19 focused on phytoplankton
(e.g., Wu et al., 2019) and 18 on ichthyoplankton (e.g., Steer et al.,
2017). Some of the publications centred on more than one taxon, 7
investigated MPs interaction with zooplankton and ichthyoplankton (e.
g, Figueiredo and Vianna, 2018), 5 with zooplankton and phytoplankton
(e.g., Chen et al., 2020), and 4 publications investigated the three
plankton groups (e.g., Faure et al., 2015) (Fig. 5). A total of 88 plankton
species were analyzed, including zooplankton, phytoplankton, and
ichthyoplankton species (Fig. 5, Table S2 – Supplementary material).
A clear preference for zooplankton was observed in studies, since 51
of the species studied were zooplankton species (Table S2 – Supple­
mentary material). More than half of zooplankton studies focused on the
freshwater cladoceran Daphnia magna (n = 31), presumably due to the
ease of maintaining laboratory cultures. From all the studies focusing on
zooplankton, 36% used copepods as a case-study, namely Acartia clausi
(e.g., Cole et al., 2013), Calanus finmarchicus (e.g., Vroom et al., 2017),
Eucalanus pileatus (Paffenhöfer and Van Sant, 1985), and Tigriopus
japonicus (Lee et al., 2013). Other groups such as Chaetognatha (e.g.,
Cole et al., 2013), Oikopleuridae (Fernández et al., 2004) and Amphi­
poda (e.g., Au et al., 2015) were also studied (Table S2 – Supplementary
material). Only 3 from the 51 zooplankton species studied were
analyzed in field studies, namely Bathochordaeus stygius (Katija et al.,
Fig. 5. Frequency of publications regarding microplastics and plankton inter­
action according to plankton groups (NB, the term ‘plankton’ denotes those
studies which did not separate the organisms into different groups).
8
Journal of Hazardous Materials 417 (2021) 126057
2017), Neocalanus cristatus (Desforges et al., 2015), and Thetys vagina
(Moore et al., 2001) (Table S2 – Supplementary material) and the
remaining species were investigated under laboratory conditions.
In contrast, there were fewer studies on ichthyoplankton and
phytoplankton, representing 16% and 15% of the publications, respec­
tively. Chlorodendraceae, Scenedesmaceae and Microcystaceae were
the main families of phytoplankton studied. A total of 22 phytoplankton
species were studied, where Chlorella pyrenoidosa (e.g., Mao et al.,
2018), Chlamydomas reinhardtii (e.g., Lagarde et al., 2016), Skeletonema
costatum (e.g., Zhang et al., 2017), and Tetraselmis chuii (e.g., Davarpa­
nah et al., 2015) were investigated more than once (Table S2 – Sup­
plementary material).
There were even fewer ichthyoplankton species studied, with only 14
different species being chosen as models to investigate the effects of MPs
on fish larvae, namely zebrafish Danio rerio (e.g., Chen et al., 2017),
marine medaka Oryzias melastigma (e.g., Cong et al., 2019), and the
Japanese rice fish O. latipes (e.g., Pannetier et al., 2019) (Table S2 –
supplementary material). Most species were used once or twice and with
different study aims thereby limiting comparisons. Six of these species of
ichthyoplankton were analyzed in field studies, namely European eel
Anguilla anguilla and Poor cod Trisopterus minutus (Steer et al., 2017) and
Atlantic bluefin tunaThunnus thynnus (Uriarte et al., 2019). Steer et al.
(2017) assessed MP ingestion rates and compared these values between
species, namely larval Anguilla anguilla, Common dragonet Callionymus
lyra, Trisopterus minutus, Thickback sole Microchirus variegatus, and
whiting Merlangius merlangus. However, and unless it was the aim of the
study, most field studies tended to combine all the organisms collected
during sampling, instead of focusing on one species or separating them
taxonomically.
3.5. Biological, ecological and ecosystem effects of MPs
3.5.1. Zooplankton
Here we emphasize the importance of discriminating between
contamination and pollution per se especially given that a biological
effect is dependent on the behaviour of the contaminant in the envi­
ronment and inside the organism and on the behaviour and biological
traits of the organism, including its ability to ingest, store and excrete
the contaminant (McLusky and Elliott, 2004). Twenty-three of the 103
laboratory studies focused on the ability of zooplankton to ingest MPs, i.
e., denoting the contamination of individuals, which could then lead to
storage or excretion together with the leaching of any toxicants from the
MPs during the passage through the organism. Murray and Cowie
(2011) found 83% of the larvae of Nephrops norvegicus, the langoustine
crustacean, collected from the field contained MPs in their stomachs,
with a predominance of filaments, whereas Zhang et al. (2019) and
Payton et al. (2020) found that most of the crustaceans collected did not
contain MPs. Even with short-term exposure or with environmentally
realistic MPs concentrations, MPs were shown to impair organism health
and cause adverse effects such as a decrease of enzymatic activity (MPs
concentrations of 0.001–0.1 mg L-1, Gambardella et al., 2017) and lower
reproduction success (MPs concentrations of 0.4 mg L-1, Peixoto et al.,
2019). Among the 103 publications analyzed, 11 report that MPs affect
zooplankton survival (n = 6, Costa et al., 2020) and growth (n = 6, e.g.,
Jeong et al., 2016) (Table 3). A few studies indicated a decrease of
fecundity (n = 4, e.g., Jeong et al., 2016) and reproductive rates (n = 5,
e.g., Peixoto et al., 2019). Other effects that indirectly affect
zooplankton survival were changes to filtration capacity (Colomer et al.,
2019), swimming activity (Gambardella et al., 2017), oxidative defence
and energy production (Tang et al., 2019) and feeding habits (Murphy
and Quinn, 2018; Wang et al., 2019) (Table 3). Physical changes and
injuries such as intestinal epithelial deformation (Wang et al., 2019) and
morphological changes (Murphy and Quinn, 2018) were also reported.
It is of note that most of these effects were observed at high MP con­
centrations (>103 mg L-1) while most studies using low MP concentra­
tions (0.001–1 mg L-1) reported limited effects (e.g., Cole et al., 2019;
S.M. Rodrigues et al. Journal of Hazardous Materials 417 (2021) 126057

Table 3 period and decreased reproduction.

Biological, ecological and ecosystem effects of MPs on three plankton groups Most studies have focused on the ability of different organisms to
(zooplankton, phytoplankton and ichthyoplankton). ingest MPs and their biological effects through exposure in the labora­
Zooplankton Phytoplankton Ichthyoplankton tory, but little is known about the role of MP in trophic fluxes. However,
Behavior • •
two publications assessed other effects such as the ability to transfer MPs
Chlorophyll content • via the food chain (Setälä et al., 2014) and to the progeny of zooplankton
Colonization of MPs • (Martins and Guilhermino, 2018). Taipale et al. (2019) demonstrated
Energy production • that zooplankton can produce, biochemically upgrade, and
Fecundity • •
trophically-transfer nutritionally important biomolecules from MPs.
Feeding •
Filtration capacity • Furthermore, Kong and Koelmans (2019) suggest that MP pollution can
Food chain transference • cause effects at the ecosystem level (affecting the critical phosphorus
Growth • • • loading) and hypothesized that the possible occurrence of catastrophic
Hatchability • cascades due to MP pollution will be predominantly driven by the
Ingestion
negative effects of MP on zooplankton.
• • •
Off-spring transference •
Oxidative defense • •
Photosynthesis activity • 3.5.2. Phytoplankton
Physical injuries • • • Among the 25 studies on phytoplankton, effects such as a decrease in
Reproduction • •
density (n = 7, e.g., Li et al., 2020a), colonization of MPs (n = 2, e.g.,
Structural changes • •
Survival/density • • • Cunha et al., 2019), and decrease of volume (n = 1, e.g., Li et al., 2020b)
Swimming activity • • were reported (Table 3). Two of the publications that investigated MPs
Volume • exposure effects on phytoplankton reported no significant effects on
growth rate, at MP concentrations of 1.472 mg L-1 (Davarpanah and
Guilhermino, 2015) and 400 mg L-1 (Lagarde et al., 2016). The
biochemical responses including the decrease of cellular esterase ac­
Ma et al., 2016). Despite the results observed in laboratory studies, tivity (n = 1, e.g., Seoane et al., 2019), decrease of lipid content (n = 1,
extrapolating to field concentrations is considered here to be non-valid, e.g., Seoane et al., 2019) and structural changes (n = 1, Yi et al., 2019)
as it requires many assumptions regarding the behaviour of the MPs both were also reported (Table 3). However, it is important to determine what
in the field and inside the organism as well as the behaviour of the or­ effects were observed according to MP type and concentration. For
ganism influencing uptake of the material. example, Chaetoceros neogracile exposed to PS beads (104 MP mL-1) did
Species used more than once as a case-study, allowed a more detailed not show an effect on its growth, morphology or fluorescence. However,
and valid comparison between studies results. For example, using sec­ an increase of MP concentration (in the region of 105 and 107 MP mL-1)
ondary MPs and a concentration between 0.4 and 1.6 mg L-1, the cala­ and using the same type of MP showed negative effects on growth,
noid copepod Artemia franciscana showed no significant effects on morphology, photosynthesis and reactive oxygen species levels (Long
growth, ingestion and mortality rates although reproductive success was et al., 2015, 2017; Seoane et al., 2019). Similarly, Chlamydomas rein­
strongly affected by the increase of MP concentrations (Peixoto et al., hardtii showed no effects on growth when exposed to primary and sec­
2019). Slightly higher MP concentrations (10 mg L-1) and using PS ondary MP (at MP concentration of 0.90 MP g mL− 1 - Lagarde et al.,
beads affected the growth of A. franciscana (Kokalj et al., 2018) and with 2016), although Li et al. (2020a) reported that the density of this
even higher concentrations (100 mg L-1) swimming and enzyme activity microalgae decreased with an increase of PS microplastics concentra­
were adversely affected (Gambardella et al., 2017). A similar pattern tions (from 5 to 100 mg L-1). Skeletonema costatum exposed to different
was observed in experiments with the copepod Calanus finmarchicus in types of polymers (in MP concentrations between 0.01 and 0.1 MP g L-1)
which PS MPs in concentrations in the region of 50 MP L-1 showed showed a significant growth inhibition, although the level of inhibition
limited affects (Cole et al., 2019) but a higher MP concentration (200 MP differed with polymer type (PVC > PS > PE) (Zhu et al., 2019).
L-1) showed significantly negative effects (such as on prey selectivity and As ecological impacts, MPs decreased photosynthetic activity (n = 2,
feeding rate) (Cole et al., 2019). Paracentrotus lividus, in contrast, e.g., Seoane et al., 2019) and chlorophyll content (n = 2, e.g., Zhao
showed no significant effects or increase of toxicity, irrespective of MP et al., 2019), thereby giving the potential to impact the marine plankton
concentration from low to high values (from 1 mg L-1) (Beiras et al., biological pump and ultimately an effect on the ocean carbon stock and
2018, 2019a,b). The different patterns observed between Artemia fran­ its fluxes (Table 3). Moreover, phytoplankton aggregation can substan­
ciscana/Calanus finmarchicus and Paracentrotus lividus showed that tially increase the microplastic sinking velocity rates and potentially be
extrapolation from one species to another is complex, and in cases where an important transport pathway (Long et al., 2015; Möhlenkamp et al.,
species have different morphologies and belong to different taxa then 2018). Hence, the presence of MPs in aquatic environments can
extrapolating effects is even more difficult. In a related note, Kokalj et al. compromise the ecological functions of these groups and the delivery of
(2018) used the same conditions (primary and secondary MPs at con­ ecosystem services such as carbon sequestration and nutrient turnover
centration of 100 mg L-1) with two species of zooplankton. Although no (e.g., de Sousa et al., 2019).
acute effects on Daphnia magna were observed, the growth of Artemia
franciscana was affected, indicating that different species respond 3.5.3. Ichthyoplankton
differently. As indicated above, Daphnia magna was the most studied Half of the 25 ichthyoplankton studies investigated the rate and
taxon and has been subjected to experiments with different MPs, poly­ ability for ingestion in fish larvae. In particular, a field study of several
mers and concentrations. D. magna suffered mortality when exposed to zooplankton and ichthyoplankton taxa (copepods, chaetognaths,
PET fibers (100 mg L-1) and the organisms were not able to recover from shrimps and fish larvae) found that fish larvae had the highest chance of
exposure (Jemec et al., 2016). Additionally, when exposed to PS sec­ encountering MPs (Sun et al., 2017). Moreover, Cong et al. (2019)
ondary MPs (400, 2000 and 10,000 MP mL− 1), D. magna showed a showed that fish larvae have no capacity to select between food and
decrease in survival, growth and reproductive rates (Schür et al., 2019). MPs. Studies that evaluated MPs effects on fish larvae, reported effects
In a related note, Ogonowski et al. (2016) compared the effects caused on survival (n = 1, Cong et al., 2019) and growth (n = 4, e.g., Xia et al.,
by primary and secondary particles (102 to 105 MP mL-1) and showed 2020) as well on reproduction (n = 1, Cong et al., 2019), and hatch­
that secondary MPs have a greater capacity to negatively affect feeding ability (n = 2, e.g., Li et al., 2019) (Table 3); these were in addition to
rates in D. magna, causing elevated mortality, increased inter-brood adverse effects that indirectly affect the survival of fish larvae such as

9
S.M. Rodrigues et al.
swimming speed (n = 3, e.g., Yang et al., 2020) and behaviour (n = 4, e.
g., Pannetier et al., 2020) (Table 3). However, it is of note that these
effects were reported using several orders of magnitude of MP concen­
tration; for example, concentrations similar to highly contaminated
environments (104 MP g-1) were shown to create an efficient egestion
and limited impact of MP on European sea bass Dicentrarchus labrax fish
larvae (Mazurais et al., 2015). Exposure to higher MP concentration
(400-500 μg L-1) and different polymers (PS, PE and PVC) showed no
significant effects or minimal impact on Danio renio fish larvae (Karami
et al., 2017; Sleight et al., 2017). It is of note that three studies that
focused on Danio renio showed no significant effects irrespective of the
degree of MP contamination (5–500 µg L-1) (Chen et al., 2017; Karami
et al., 2017; Sleight et al., 2017). Similar conditions also did not produce
negative effects on consumption or growth on Fathead minnow Pime­
phales promelas fish larvae (Malinich et al., 2018). In contrast, Lönnstedt
and Eklöv (2016) observed a decrease of hatching and growth rates and
alteration of feeding preferences in larval perch Perca fluviatilis at an MP
concentration of 103 MP m-3. Furthermore, Lönnstedt and Eklöv (2016)
found that fish larvae exposed to MPs do not respond to olfactory threat
cues, confirming that the negative effects of MPs operate both chemi­
cally and physically, which increases the predator-induced mortality
rates. Experiments with secondary MPs at concentration of 70–7000 MP
L-1 showed negative effects on Oryzias latipes; these include morpho­
logical changes to head/body ratio and decreases in swimming speed
coupled with an induction of EROD activity (involved in detoxifying
complex contaminants) and DNA strand breaks (Pannetier et al., 2019;
2020). In a related note, effects on survival and growth as well as effects
on reproduction and hatchability were reported using high level of PS
MPs (105 MP L-1) on Oryzias melastigma (Cong et al., 2019; Li et al.,
2019) as well as oxidative stress, increased heart rate, and swimming
speed on Goldfish Carassius auratus fish larvae (Yang et al., 2020).
The literature analyzed shows that a degree of contamination similar
to that found in highly contaminated environments can either not cause
negative effects in some fish larvae species or cause effects such as a
decrease of growth, alteration of behaviour and feeding preference in
others. Therefore, as different species can have different behaviours,
biological traits and morphologies, then it is difficult if not invalid to
extrapolate the effects observed in one species to another. Finally, given
that most of the experiments that focused on ichthyoplankton were
performed with PS particles and only a few used secondary MP, PVC and
PE, it is not possible to determine whether different polymers will have
different effects on these organisms. This emphasizes the need for more
studies with more species and polymers and with lower (environmen­
tally realistic) MPs concentrations.
4. Knowledge gaps – future work
4.1. Lack of field studies
Although there is an increase in MP contamination field studies and
especially those in the sea, many geographical areas and other ecosys­
tems require further study to provide valid comparisons of the size and
nature of the problem caused by MPs. Furthermore, while laboratory-
studies are essential in understanding the ability of an organism to
ingest MPs and their effects, the biological effects of MPs present in the
environment in the smaller organisms are still poorly known since there
are many factors that can affect the results and restrict identifying the
effect of a single variable. As shown here, while there are many studies
on ingestion of MPs by zooplankton or adsorption onto phytoplankton
leading to organism contamination, further studies are required partic­
ularly to determine the repercussions of that contamination at all levels
of biological organization in the field, from the cell through individuals
and their populations, to communities and the ecosystem as a whole.
Another gap in field studies is the lack of a standardized methodol­
ogy. Studies in different locations tend to use different techniques and/
or express results in different units. For example, MPs concentration are
10
Journal of Hazardous Materials 417 (2021) 126057
usually and variously expressed as particles per volume filtered, parti­
cles per area covered or weight, thereby making comparison with lab­
oratory results difficult. As a further variable, as shown by the studies
interrogated, the colour of the MP needs to be considered. Although
their study was carried out in freshwater, which has different optical
properties from the sea and estuaries, Xiong et al. (2019) detected
changes attributed to color in ingestion by fishes. Hence it is emphasized
that the lack of a standard methodology precludes valid comparisons
between studies.
4.2. MPs used in lab studies need to be more representative of those found
in the environment
The analysis here indicated that, in general, MPs concentrations used
in laboratory studies are much higher than ambient environmental
concentrations, reaching 106 and even 109 MPs m-3, i.e., approx. 4500
times greater than the highest field concentration reported. As such, it is
not valid to extrapolate from experimental to field effects and so there is
the need to use more environmentally relevant MPs concentrations in
laboratory studies and in environmental risk assessments. Furthermore,
there is the need to standardize the concentration, polymer, and shape of
MPs used. Most studies on the bioavailability and effects of microplastics
used specific types of MPs (notably PS and PE spherical particles) that do
not necessarily coincide with polymers most commonly found in aquatic
environments. Similarly, the experiments usually used ‘virgin’ MPs
which had not been ‘weathered’, i.e., exposed to environmental condi­
tions which otherwise could have affected their surface properties and
biofilm coatings by diatoms, bacteria, and fungi such as yeasts; the latter
would have increased the palatability of the MPs.
Some studies included in this systematic review highlight that the
form of MPs can change with exposure to environmental conditions, and
also the type of MPs should be taken into consideration since it is
apparent that, for example, fibers rather than beads tended to impair the
health and ecological functions of the organisms; in addition, under
continuous exposure these inhibited food assimilation (Blarer and
Burkhardt-Holm, 2016). Other studies emphasized that shape could
influence MPs bioavailability, since PA fibers showed significantly
negative effects, such as an alteration in prey selectivity, compared to PA
beads that showed non-significant adverse effects (Cole et al., 2019).
These results emphasize the need for a greater simulation of field con­
ditions in laboratory experiments, thereby increasing the validity and
comparability of biological responses to those in aquatic environments.
4.3. Phytoplankton and ichthyoplankton should receive more attention
It is of note that compared to zooplankton, which were the subject of
2/3 of the publications, the other groups of plankton are largely un­
derrepresented in previous studies. While fish are well represented in
their adult stage, little information is available regarding their early life
stages, their most sensitive stage which highly influences annual
recruitment to adult populations. Similarly, the effects of MPs are not
consistent between plankton groups nor even among species and
although 88 species were studied, many taxa are under-represented,
specifically, ichthyoplankton and phytoplankton. Larvae of economi­
cally important fish or crustaceans or even other trophically-important
plankton groups such as chaetognaths or dinoflagellates should be
considered as future case studies. Since different species can be impacted
in different ways by MPs, according to their morphology, behaviour, and
characteristics, it is difficult to extrapolate the effects observed in one
species to another. Although contamination and the resulting trophic
transfer have been observed in zooplankton, especially with nano­
plastics, thereby potentially affecting higher trophic levels, there is the
need for further studies to quantify these aspects.
S.M. Rodrigues et al.
4.4. Lack of information regarding MPs effects on populations and
ecosystems
Despite the many studies in other groups on the effects of contami­
nants at all levels of biological organization, from the cell to the
ecosystem, and on all aspects of biological structure and functioning (e.
g., physiology, biochemistry, morphology, disease and anomalies, ge­
netics, production ecology, etc.) (e.g., McLusky and Elliott, 2004; Gar­
cía-Alonso et al., 2011), many of these aspects have not been addressed
in plankton with regard to MPs. Although there are inter- and
intra-specific differences in the potential impacts of MPs in plankton
groups, negative effects on growth, survival, physical impacts, repro­
duction, and feeding are relatively well-established, but MPs ecological
and ecosystem effects are still poorly known. For example, biological
and individual effects may negatively affect primary and secondary
productivity, but this needs further study (Troost et al., 2018). There
also needs to be studies on the weathering and biofilm generation effects
on MPs, for example with increasing time in the environment the MPs
may have a greater biofilm which will influence its uptake.
Effects at higher levels of biological organization cannot be deter­
mined without multi-generational and multi-trophic level studies. The
review here showed that most studies focused on individual effects, but
community and ecosystem effects are relatively lacking and the impact
of MPs in ecological functions (e.g., photosynthesis, primary production,
predator-prey interactions) are still scarce. Similarly, there are few
studies on the transfer of the contaminants and their effects between
generations (from parent to progeny) and from prey to predator; these
aspects need to be studied to indicate the population, community and
ecosystem effects. Future studies should also integrate MPs pollution in
ecological models to help understand the ecosystem effects. While in
marine pollution studies in general, it is assumed that effects at the
cellular and individual levels of biological organization will get trans­
ferred to the population, community and ecosystem level, this is rarely
the case given that the ‘signal’ of such lower level effects gets absorbed
by the variability and complexity of the whole system, a feature termed
environmental homeostasis (Elliott and Quintino, 2007). This feature
has not yet been studied in plankton systems in relation to MPs
contamination and yet it urgently needs addressing.
The analysis here has showed that a few publications focused on
impacts other than biological and individual ones, such as changes in
faecal pellet production and aggregation that lead to quicker precipi­
tation of MPs and their increased density on the seabed (e.g., Long et al.,
2015; Cunha et al., 2019) or the ability as the result of consumption and
excretion to degrade MPs (Dawson et al., 2018; Hodgson et al., 2018).
Further information on these aspects would emphasize the long-term
effect on pelagic food webs but also indicate the overall sequestration
of MPs; for example, while zooplankton are well known for their ability
to ingest petroleum oil droplets and deliver the contaminant in faeces to
the seabed (McLusky and Elliott, 2004), this feature needs to be further
quantified for MPs. Further research on the way in which the presence of
MPs can alter the organism behaviour is essential to understand the
impact on the population especially the need to understand how the
possible decrease of these populations will affect the community and
ultimately the ecosystem. This emphasises the need for studies that
interrogate the mechanisms of interactions between MPs and ecosys­
tems at the different biological levels of organization and at different
spatial and temporal ecological scales.
5. Conclusions and lessons learned from the literature search
The current study accessed many relevant papers, but the search
could be expanded by including the ever-increasing terms related to
microplastics research. This could include adding recent terms and
alternative spellings such as the words synthetic(s), fiber/fibre and
nanoplastics. Similarly, it is of note that some very recent papers refer to
the type of plastic and/or synthetic material as a specific type of polymer
11
Journal of Hazardous Materials 417 (2021) 126057
(such as polystyrene) and the many types of synthetic material could be
also used in the search string. These terms were not included in the
current review, but our findings suggest that this does not materially
affect the conclusions reached. Similarly, it is likely that all literature
searches do not find the more inaccessible and often grey literature, but
the present study appears to have accessed the main literature.
The systematic review here allowed the testing and acceptance of the
original premise, that more studies relate to contamination, i.e., the
presence of the MPs, rather than to pollution per se, as an adverse bio­
logical response at various levels of biological organization resulting
from environmentally realistic levels of MPs in the environment. In
particular, while impacts on the health and survivability of the indi­
vidual planktonic organisms (i.e., pollution per se) were found in labo­
ratory studies, field studies were more focused on contamination.
The review highlighted that many publications were laboratory-
based studies and focused on zooplankton species. Effects on other
plankton groups, namely phytoplankton and ichthyoplankton, remain
less known. To allow the extrapolation of laboratory-based results to the
environment, it is necessary that laboratory conditions mirror the field
conditions. However, a dissimilarity and non-comparability between
laboratory and field conditions was observed, especially in experimental
conditions, MP characteristics and concentrations. It would be more
relevant to better define laboratory exposure conditions and mimic
environmental conditions that would be more consistent with the nat­
ural environment and thus allow translation into realistic biological
effects. In particular, an effort needs to be made on increasing field
studies, especially on the community and ecosystem effects of MPs
pollution.
CRediT authorship contribution statement
Sabrina M. Rodrigues: Conceptualization, Formal analysis, Inves­
tigation, Methodology, Writing - original draft. Michael Elliott:
Conceptualization, Supervision, Writing - review & editing. C. Marisa
Almeida: Conceptualization, Funding acquisition, Investigation, Su­
pervision, Writing - review & editing. Sandra Ramos: Conceptualiza­
tion, Methodology, Funding acquisition, Investigation, Supervision,
Writing - review & editing.
Funding sources
This study was partially supported by FCT - Foundation for Science
and Technology within the scope of UIDB/04423/2020 and UIDP/
04423/2020 and a PhD fellowship to SM Rodrigues (SFRH/BD/145736/
2019).
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgements
The authors wish to thank three anonymous referees for their
insightful and substantial comments on earlier versions of the paper.
Appendix A. Supporting information
Supplementary data associated with this article can be found in the
online version at doi:10.1016/j.jhazmat.2021.126057.
S.M. Rodrigues et al. Journal of Hazardous Materials 417 (2021) 126057

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