Received: 7 September 2020 | Revised: 31 December 2020 | Accepted: 22 February 2021

DOI: 10.1111/gcb.15570

RE S E A R C H RE V I E W

Microplastics and the functional traits of fishes: A

global meta-analysis

Martina Salerno1 | Manuel Berlino1,2 | M. Cristina Mangano3 | Gianluca Sarà1

1Dipartimentodi Scienze della Terra e del

Mare (DiSTeM), Università degli Studi di
Palermo, Palermo, Italy
2NationalInstitute of Oceanography and
Applied Geophysics – OGS, Trieste, Italy
3Stazione Zoologica Anton Dohrn,
Department of Integrative Marine Ecology
(EMI), Sicily Marine Centre, Palermo, Italy
Correspondence
M. Cristina Mangano, Stazione Zoologica
Anton Dohrn, Department of Integrative
Marine Ecology (EMI), Sicily Marine
Centre, Lungomare Cristoforo Colombo
(complesso Roosevelt), 90149 Palermo,
Italy.
Email:
Funding information
Ministry of Italian Research, Grant/Award
Number: 2017MHHWBN_003; Sicilian
Region and Maltese Government, Grant/
Award Number: C1-3.1-31; National
Institute of Oceanography and Applied
Geophysics; European Union's Horizon
2020, Grant/Award Number: 835589
Abstract
Over the years, concern about the effects of microplastics has grown. Here, we an-
swered the main question “What are the impacts of microplastics on the functional
traits of fish species?” through a meta-analysis. The general impact of microplastic
exposure on the functional traits of fishes and specifically on eight variables, namely,
behaviour, development, fecundity, feeding, growth, health, hatching and survival
was explored. Subgroup analyses were performed to detect correlations between the
im- pact of microplastics and the following factors: species, life stage, habitat, water
col- umn habitat, day of exposure to microplastics and microplastic size, type and
shape. A meta-regression analysis allowed understanding the correlation between
the impact of microplastics and the size of organisms. Generally, microplastics have
a negative effect on the functional traits of fishes. Feeding and behaviour, followed
by growth showed the greatest impact. Among the subgroup analysis, four of the
eight variables considered showed a significant difference between groups: species,
life stage, mi- croplastic shape and days of exposure to microplastics. Depending on
their life stage, organisms may be more sensitive to microplastic pollution. Changes
in growth rates, development of early life stage and behavioural patterns in fishes
may have a nega- tive effect on the structure and functions of aquatic ecosystem in
the long term and consequently affect the ability of aquatic ecosystems to provide
ecosystem services and sustain human communities.

K E Y WO R D S
effects size, fishes, functional traits, meta-analysis, microplastics

1 | I NT RODUC TION
The accumulation and fragmentation of plastics represent one of
the most recent, ubiquitous, long-lasting and warning signals for our
planet. Within just a few decades, since mass production of plastic
products, plastic debris have accumulated, from terrestrial environ-
ments, in the open oceans and even the most remote environments
such as the deep-sea floor (Galgani et al., 1996; Kane et al., 2020).
Microplastics are typically defined as plastic pieces of <5 mm in
size
Martina Salerno and Manuel Berlino contributed equally to this work sharing the first
co-authorship.
primarily derived from larger plastic items that are crumbled in the
environment as a consequence of prolonged exposure to UV light
and physical abrasion (Andrady, 2003; Thompson et al., 2004).
Microplastics have been documented in all aquatic systems from
both marine and freshwater habitats (Barnes et al., 2009), on
beaches (Browne et al., 2011), sediments (Claessens et al., 2011)
and ubiqui- tously along the water columns (Eriksen et al., 2013).
The sources of microplastics found across all ecosystems vary and
include food or drink containers, packaging, fibres from synthetic
clothing, indus- trial waste and microbeads (components of some
beauty products; Biginagwa et al., 2016; Kershaw & Rochman,
2015).

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Over the years, plastic pollution has become a growing con-
cern. Jambeck et al. (2015) calculated that 275 million metric tons
(MT) of plastic waste was generated in 192 coastal countries (93%
of the global population) in 2010, with 4.8–12.7 million MT en- tering
the ocean. A part of these plastic debris floats on the sea surface.
Eriksen et al. (2014) estimated that at least 5.25 trillion plastic
particles weighing 26,894 tons were floating in the world's oceans
and 3554 tons of these were microplastics, whose early detection
through spectral characterisation is promising (Corbari et al., 2020).
The vast majority of plastic ends up in the deep sea. The seafloor
can be considered as a hotspot of microplastic pol- lution, exhibiting
the highest densities in the order of up to 1.9 million particles per m 2
(e.g. Tyrrhenian Sea), which is driven by near-bed thermohaline
currents (bottom currents), assembling ex- tensive seafloor
sediment accumulations (Kane et al., 2020). These currents supply
oxygen and nutrients to deep-sea benthos, sug- gesting that deep-
sea biodiversity hotspots are also likely to be microplastic hotspots
(Azpiroz-Zabala et al., 2017; Davies et al., 2009). Based on these
data, it could be assumed that the highest amount of plastic per
individual may well be found in benthope- lagic fish.
The number of studies examining the potential impacts of mi-
croplastics on aquatic ecosystems, marine species and food webs
has increased exponentially (Bucci et al., 2020; Lusher et al., 2017).
Microplastics have been found in the digestive tracts of both farmed
and wild-caught fish (Foekema et al., 2013; Ma et al., 2020; Phillips
& Bonner, 2015) and aquatic invertebrates (Cole et al., 2011).
Organisms may actively ingest microplastic particles, confusing
them with prey (Savoca et al., 2017), or passively during particle fil-
tration (Collignon et al., 2014). Azevedo-Santos et al. (2019)
reported plastic ingestion by 427 fish species (mostly marine
species) from different regions, ecosystems and guilds.
After ingestion, microplastics can remain in the digestive tracts
of organisms from days to weeks (Batel et al., 2016; Browne et al.,
2008). This uptake/ingestion, retention and egestion/elimination of
microplastics—kinetic processes and exposure to microplastics from
both diet and water—could adversely affect the health of organisms
(e.g. gastrointestinal tract). Yin et al. (2019) found that microplastic
exposure altered behavioural traits, energy reserves and the nutri-
tional quality of demersal black rockfish. However, some studies
have concluded that microplastics have no effect on organisms, un-
less associated with organic contaminants (Le Bihanic et al., 2020;
Schmieg et al., 2020).
Here, we classified a multitude of studies and different related
outputs by extracting and synthesising data available in the litera-
ture. In order to reply to the main question: “What are the impacts of
microplastics on functional traits of fish species?” we conducted a
meta-analysis examining the impacts of microplastic exposure on
the functional traits of fishes. We focused on the functional traits
because most prominent ecological research conducted in the last
two decades definitively assigns a primary role to functional traits as
the shaping forces of population dynamics and ultimately eco-
system functioning (Sibly et al., 2012). By functional, here we refer
SALERNO
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to “morpho-physio-phenological traits which impact fitness indi-
rectly via their effects on growth, reproduction and survival, the three
components of individual performance” (Violle et al., 2007,
p. 882). Performance traits have been included in our meta-
analysis (Arnold, 1983). In fishes—the main target of this study
constitut- ing the vast majority of organism biomass in aquatic
habitats and food items largely included in human consumption—
these traits usually include tolerance and sensitivity to
environmental condi- tions (e.g. Kearney & Porter, 2009). These
latter limit the ability of each species to maintain its metabolic
machinery (Sarà et al., 2014; Sokolova et al., 2012), to obtain
energy from food, and all other behavioural traits such as
swimming behaviour, habitat use, the mating system and
morphological (e.g. shape) traits (Schoener, 1986), allowing
optimisation of energetic income (Krebs & Davies, 1987). Thus, to
gain insight on the effects of any potential distur- bance factor, such
as microplastics on the functional traits of fishes, it is crucial to
increase our understanding of how microplastics can impair basic
functions (as expressed by organismal functional traits; Violle et
al., 2007) of ecological functioning. Several perspective and
opinion papers have tried to shed light on the effects of micro-
plastic pollution on the biotic components of aquatic systems and
attempted to summarise the accumulated knowledge (Al-Thawadi,
2020; Pirsaheb et al., 2020). So far, however, efforts to synthesise
available data through meta-analytical quantitative approaches
are limited (Foley et al., 2018). Nonetheless, meta-analyses allow
quantitative assessment of the effect of a given treatment (in this
case, exposure to microplastics) over multiple studies conducted
using different experimental procedures, on different species, and
by different research groups and to summarise and understand the
broader potential impacts of the treatment in question. Foley et al.
(2018) examined the impacts of the exposure of fish and aquatic
in- vertebrates to microplastics, considering four responses:
consump- tion and feeding, growth, reproduction and survival.
They assessed whether the effects are consistent across different
taxonomic groups or plastic shapes, and examined whether the
size of the ef- fect varies with experimental conditions. By including
only exper- imental and manipulative studies, we wanted to reach
beyond the common aims found across the current literature, which
evaluate the general impact of microplastic exposure on the
functional traits of all fishes and to increase the number of
variables examined by Foley et al. (2018), investigating: four
functional traits—behaviour, development, feeding, hatching—and
three performance traits— fecundity, growth, survival (as from
Arnold's, 1983 framework re- visited by Violle et al., 2007). An extra
category named “Health” was created to group variables commonly
find out into the retrieved literature assessing fish health status
(Table 1). Through subgroup analyses, we explored whether there
is a correlation between the impact of microplastics and many
other factors (e.g. species, life stage, habitat, water column habitat,
microplastic size, type, shape and days of exposure). Moreover,
given that body size is the major trait driving individual fitness
(Barneche et al., 2018), we explored the correlation between the
impact of plastic and the body size of fishes.
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TA B L E 1 List of the eight response categories examined in our meta-analysis, the associated description/quantification and the measured
variables used (keywords) in the selected studies. Specifically, the four functional traits—behaviour, development, feeding, hatching—the
three performance traits—fecundity, growth, survival—as from Arnold's (1983) framework revisited by Violle et al. (2007), and a last
category dealing with ‘health’, commonly found in the retrieved literature. Regarding the quantification of variables, we followed the
quantification reported by the authors, according to the methods applied by them
Trait Description/Quantification
Functional traits
Behaviour Organisms' behavioural changes reported after
ingestion or exposure to microplastics in
comparison to an unexposed control group
Development Capability to grow specific part of the organisms or to
complete transformation stages after exposure to
microplastics and in comparison to an unexposed
control group
Feeding Feeding activity of organisms in the presence of
microplastics and in comparison to an unexposed
control group
Hatching Variation in the egg hatching phase after exposure to
microplastics and in comparison to an unexposed
control group
Performance traits
Fecundity Variation in egg production and fertilisation after
exposure to microplastics and in comparison to an
unexposed control group
Growth Variation in organismal size in the unit of time measured
after exposure to microplastics and in comparison to
an unexposed control group
Survival Survival rate of organisms exposed to microplastics and
in comparison to an unexposed control group
Health Changes in general organism health state after
exposure to microplastics and in comparison to an
unexposed control group
aForthose studies reporting mortality percentage, where possible, these measures have been converted into survival percentage, so that the values
reported for this category were exclusively survival measures.
2 | MAT ERI AL S AND MET HO DS
2.1 | Literature search and data collection
The scientific papers included in our meta-analysis were collected
by performing a literature search (Moher et al., 2009; Pullin &
Stewart, 2006) aimed at answering our main question. A complex
search string was used on the two main literature databases, ISI
Web of Knowledge (Web of Science Core Collection package,
Clarivate Analytics, 2019) and Scopus, with no temporal scale
restriction. The search string was:
(("microplastic*" OR "micro plastic*" OR "micro-plastic*") AND
("trait*" OR "function*" OR "response*" OR "measure*" OR "rate*"
OR "Behaviour" OR "Feeding" OR "Growth" OR "Health" OR
"Hatching" OR "Survival") AND ("laboratory" OR "mesocosm*" OR
"experiment*" OR "treatment*") AND ("*fish*")).
The search string was created to include four main elements of
our primary question (linked by the Boolean operator ‘AND’; Moher
et al., 2009; Pullin & Stewart, 2006), respectively: the exposure (i.e.
microplastic and related keywords), the measured outcomes (i.e.
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Measured variables (keywords)
Activity rate, locomotor activity, mobility, swimming velocity,
maximum velocity, distance travelled, spontaneous
movement, turning behaviour, inactivity
Biometric measurements, head length, head height, head
depth, liver weight, gill weight, gonad weight, swim bladder
area, optic vesicle area, pericardium area, angle between
myosepts, distance between myosepts, interocular
distance
Predatory performance, feeding success, foraging time, number
of ingested prey
Hatching per cent, hatching success, hatching rate, hatching
time
Egg production, fertilisation rate
Body weight, body length, standard length, total length, weight
gain rate, body mass, changes in body mass, length–weight
ratio
Survival rate, survival percentagea
Condition factor, hepatosomatic index, gonadosomatic index,
heartbeat, mucus secretion, oxygen consumption
traits and related keywords), the target population (or subject of the
search, i.e. fish) and the observation type (e.g. laboratory and re-
lated terms). This latter group of keywords was added to avoid the
inclusion of the large number of studies reporting only the micro-
plastic occurrence in the field with not associated measured effects
reported (details on the search string creation strategy are reported
in Table S1). The measured outcomes, list of traits taken into exam,
an associated description/quantification and the measured variables
used (keywords) in the selected studies are in Table 1. All the syn-
onymous were linked by the Boolean operator ‘OR’. By running the
search string (final search date 20 May 2020; Table S1) and after
checking for duplicates (Figure S1), we obtained 208 scientific peer-
reviewed papers. Spurious results were removed, for example stud-
ies concerning environmental microplastic pollution, description of
microplastic extraction methods and microplastic effects on several
aquatic organisms other than fish, from zooplankton to benthic or-
ganisms (Table S2). Given that our study aimed at testing the global
effects of microplastics on fish species, we considered species from
all the water realms (i.e. freshwater, marine and estuarine) and fish
specimens at any life stage (i.e. from the embryo stage to adults).

2648 | AL.
We selected those studies that clearly compared experimental treat-
ment groups against one or more controls (i.e. group of organisms
exposed to microplastics tested against untreated organisms) and
those studies that reported the mean values of the measured func-
tional trait variables, the number of replicates and a measure of the
variability around the mean (Table S3). We selected those studies
focusing on the effects of microplastics on the functional traits of
fishes, measurable at individual level, and variables that had direct
effect at population level. The functional traits that we focused on
included morphological (e.g. body length), physiological (e.g.
hepato- somatic index, respiration) and behavioural (e.g.
swimming activity)
traits (Arnold, 1983; Violle et al., 2007). These traits are usually in-
volved in the optimisation of individual fitness and have effects at
the population level, such as growth and mortality response. Thus,
we excluded all observational studies, that is studies assessing the
presence and concentration of ingested microplastic polymers or
those using pollutants or other chemical compounds (e.g.
antibiotics) added to microplastics, and those focusing on the
effects at the sub- organismal level (e.g. studying cellular and
subcellular variables such as oxidative stress, gene expression,
immunological responses, etc.).
Reviews, analyses on the effect of nanoplastics and papers not
re-
lated to the functional trait of fish or with insufficient data were also
excluded (see the list of excluded studies in Table S2). By
applying
such selection criteria, we selected only those with a clear descrip-
tion of experimental design, such as comparisons of experimental
treatment groups with one or more control groups (i.e. a group of
organisms exposed—‘treated’—to microplastics tested against not
exposed organisms, ‘untreated’). Our final datasets included 43 sci-
entific papers that were considered suitable for our analysis (Table
S3; Figure S1 reporting the adapted PRISMA flow diagram; Moher
et al., 2009).
2.2 | Calculation and analysis of effects
Due to the different variables and approaches adopted in the se-
lected scientific papers, we used the Hedges' g statistic, which is
the bias-corrected standardised mean difference between the treat-
ment and control groups, divided by the pooled standard deviation
(Hedges, 1981; Sarà, 2007). The Hedges' g value and its variance
were calculated for each case study (k = 754 total case studies
within our dataset) in order to estimate the difference in the effects
of mi- croplastics between an experimental treated group and a
control group. Hedges' g weighs cases by their sample size and the
inverse of their variance (Borenstein et al., 2011). The value of
Hedges' g ranges from −∞ to +∞ and can be interpreted as follows
(sensu Koricheva et al., 2013): |g| ≤ 0.2 considered a small effect;
0.2 ≤ |g| ≥ 0.5 a me- dium effect; 0.5 ≤ |g| ≥ 0.8 a large effect; and
|g| ≥ 0.8 a very large ef- fect. The effect size Hedges' g was
calculated as follows (Borenstein et al., 2011):
‼ ‼
( Y t− Y c)
Hedges � g = × J,
standard deviation pooled
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where Yc and Yt are the mean of the control and experimental treat-
ment groups respectively.
The correction for bias attributed to different sample sizes, repre-
sented by J, was estimated through differential weighting as follows:
3
J = 1 − 4 ( N + N − 2) − 1 .
t c
The following formula was used to calculate the pooled standard
deviation (standard deviation pooled):
( N − 1) × SD2 + ( N − 1) × SD2
t t c c
,
Standard deviation pooled =
Nt + Nc − 2
where N is the sample size and SD is the standard deviation of the
treated or control group. In order to account for inequality in study
variance, effect sizes have been weighted using the inverse of the
sam- pling variance, therefore calculating variance for each effect size
(Vg) as
follows (Koricheva et al., 2013):
Nt + Nc g2
= +
Vg
ntnc .
2( nt nc )
As the sign of Hedges' g tells the direction of the effect, a neg-
ative value of Hedges' g indicates that microplastics have a higher
effect on impairing that specific analysed response.
In order to measure the effect size on single response variable
and to minimise the high heterogeneity of the dataset, we used be-
haviour, development, fecundity, feeding, growth, health, hatching
and survival as eight response categories (Table 1). Therefore, we
run a model estimating overall effect size and 95% CI per category.
To investigate possible differences in the pooled effect size
among tested variables related to the biology and ecology of
fishes or to the experimental conditions of exposure to microplas-
tics, we performed subgroup analysis. Such an analysis included
the following categorical fixed factors as moderators of the mixed-
effects model: habitat (freshwater, marine and estuarine), water
column habitat (pelagic, benthopelagic and demersal), species
(dif- ference in the effects at individual level), life stage of fishes
(em- bryos, larva, juvenile, adult), microplastic type (difference in
the effects depending on the use of a mix of microplastics or
different types of polymers), microplastic shape (fibres,
fragments, spheres), microplastic size (<25, 25–100, 100–500,
>2000 µm) and days of exposure (from less than a day to more
than 90 days) subgroups.
Finally, to investigate the possible correlation between the di-
mension of the organisms (total length, mm) on different life stages
and the effect of microplastic on traits, we run meta-regression
analysis with mixed-effects model including organism size (total fish
length expressed in mm) retrieved from the studies included in our
meta-analysis as continuous fixed factor.
The meta-analyses were conducted using the metafor pack-
age for R (Anton et al., 2019; Viechbauer, 2010). We performed
mixed-effects models using the ‘rma.mv’ function which uses a
SALERNO
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Wald-type test to determine statistical significance. We ran the sta-
tistical model that included the study identification number (i.e. Id of
the study in our dataset) and the response variable (i.e. functional
trait categories) as a random factor to account for heterogeneity
(Viechtbauer, 2007) and non-independence of results from the same
study (Konstantopoulos, 2011).
Effect sizes for the models including categorical fixed factor
were considered to be significant if their 95% confidence interval
(CI) did not overlap with zero and if their p ≤ 0.05. For the model
with a continuous fixed factor (i.e. length of the organisms, mm), the
predictor was considered to be significant at p ≤ 0.05. Differences
between the groups included as moderators in the subgroup analy-
sis were considered to be significant when the p-value of the test for
moderators (Q m) calculated in the mixed-effects model was ≤0.05.
2.3 | Publication bias
Results in meta-analysis might be distorted by publication bias,
which is the selective publication of articles finding significant
effects over those that find non-significant effects (Koricheva et
al., 2013). Our analysis could result in an overestimate of the
effects of microplastics on the functional traits due to the publi-
cation bias that was evaluated using Egger's regression test
(Egger et al., 1997) by running models that included the standard
error of the effect sizes (included as the square root of the
variance) as a moderator (Habeck & Schultz, 2015). Potential
publication bias was determined when the intercept of the model
was different from zero at p ≤ 0.05 (Anton et al., 2019). If potential
bias was detected, we examined the data for potential outliers by
looking at the effect sizes with standardised residual values
exceeding
FI G U R E 1 Forest plot of the overall
effect size and individual response variable
effect size. Analysis conducted with mixed-
effects model, using the rma.mv function
of the metaphor package in R, including
study Id and functional trait as random
factor. Black boxes represent Hedges' g
value and the horizontal lines represent
the 95% CI for each g value; Q m = omnibus
test of moderators from the model; k =
number of study cases [Colour figure can
be viewed at wileyonlinelibrary.com]
| 2649
the absolute value of three (Viechbauer et al., 2010) using the
rstandard function in R. Potential outliers were removed to adjust
for publication bias. Adjusting for publication bias did not change
the outcome of the analyses (by comparing fitted random-effects
models with and without the influence of the potential outliers),
except for the effects of microplastics on growth, freshwater
species, benthopelagic and demersal species, embryos and lar-
vae life stage and the species Dicentrarchus labrax, Perca fluvia-
tilis and Sebastes schlegelii (Table S4). We then removed from
the dataset the potential outliers detected in the sensitivity
analysis and re-ran the mixed-effects models to evaluate the
effects of microplastics on the different variable analysed.
Otherwise, the sensitivity analyses showed that our results of the
models were robust against publication bias (detailed information
on sensitivity analysis reported in Table S4).
3 | RESULT S
The current analysis included 754 case studies obtained from the
43 selected papers (details of the included studies, that is variables
associated with the studies and number of case studies, are
reported in Table S3).
The overall analysis conducted by mixed-effects model on
the entire database (including all the individual response vari-
ables) showed a medium negative effect size (g = −0.25 ± 0.14;
***p < 0.001; Figure 1). This result shows an overall effect of mi-
croplastics on fishes causing a decrease of mean response variable
respect to the controls.
Concerning the response variables, three out of eight (specifically
behaviour, feeding and growth) showed a significant effect (Figure 1).

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3.1 | Subgroup analysis
A significant difference between groups was found for four of the
eight considered variables, specifically, species, life stage,
microplas- tic shape and days of exposure to microplastic
subgroups. For spe- cies, the analysis revealed significant
differences between species subgroups (Q m = 66.04, ***p < 0.001)
suggesting that the effect of microplastics on an individual's
functional traits varies as a function of the species. The mixed-
effects model analysis within subgroups revealed significant effect
size for six out of 19 species with the ef- fect varying from positive to
negative, and small to very large (see Figure 2 for major details).
Embryos, larvae, juvenile and adult groups appeared to be
significantly different (Q m = 8.52, *p = 0.03). Our mixed-effects
analysis within subgroups showed a medium negative effect of
microplastics on juveniles (g = −0.47 ± 0.24, ***p < 0.001). No sig-
nificant effect was detected within the other life stage subgroups
(Figure 3).
An investigation of possible differences according to habitat in
general and the water column in particular did not identify signifi-
cant differences between subgroups (Figure 3).
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The analysis conducted on the experimental conditions revealed
significant differences between subgroups of microplastic shape
(Qm = 9.31, *p = 0.02) and between subgroups of days of exposure
to microplastics (Q m = 20.29, **p = 0.005; Figures S2 and S3). The
analysis within subgroups showed a medium negative effect size for
all three microplastic shape: fibres (g = −0.53 ± 0.47, *p = 0.02),
frag- ments (g = −0.42 ± 0.30, **p = 0.006) and spheres (g = −0.30
± 0.26,
*p = 0.02). Regarding the time of exposure to microplastics, the
analysis within subgroups showed: medium negative effect size for
8–14 days of exposure (g = −0.41 ± 0.29, **p = 0.006); medium neg-
ative effect size for 15–21 days (g = −0.55 ± 0.30, ***p = 0.001);
medium negative effect size for 22–30 days (g = −0.41 ±
0.39,
*p = 0.03); large negative effect size for 61–90 days (g = −0.68 ± 0.46,
**p = 0.004). No significant differences were detected between
groups of microplastic type or size (Figure S2).
The results of the meta-regression did not indicate any variation
of the effect size in correlation with the size of the organisms regard-
less of the life stage (p = 0.25, ns). These results remained
unchanged for the juvenile (p = 0.23, ns) and adult life stages (p =
0.11, ns), while being significant (**p = 0.007) for the larval life stage
with the effect size becoming more negative as the larval size
increased (Figure 4).
FI G U R E 2 Forest plot of the ‘Species’
subgroup effect size. Analysis conducted
with mixed-effects model, using the rma.
mv function of the metaphor package in R,
including study Id and functional trait as
random factor. Black boxes represent the
Hedges' g value and the horizontal lines
represent the 95% CI for each g value;
Qm = omnibus test of moderators from the
model; k = number of study cases
SALERNO Et AL. | 2651
FI G U R E 3 Forest plot of the (a)
‘Habitat’, (b) ‘Water column habitat’ and
(c) ‘Life stage’ subgroups effect size.
Analysis conducted with mixed-effects
model, using the rma.mv function of the
metaphor package in R, including study
Id and functional trait as random factor.
Black boxes represent the Hedges' g value
and the horizontal lines represent the 95%
CI for each g value; Q m = omnibus test of
moderators; k = number of study cases

FI G U R E 4 Meta-regression showing
relation of effect size and organism
size (total length expressed in mm).
Analysis conducted with mixed-effects
model, using the rma.mv function of the
metaphor package in R, including study Id
and functional trait as random factor. The
size of the point is related to the standard
error of the study; dotted lines indicate
95% CI

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4 | DI SCUSSIO N
Our results showed that microplastics have a general negative effect
on the functional traits of fishes regardless of habitats and species.
Regarding the analysis as a whole, which includes all the hetero-
geneous data, the effect size appears to be statistically significant
and negative. Moreover, all the single response variables, that were
statistically significant, exhibited a negative effect size. Compared
to the Foley et al. (2018) study, our meta-analysis has confirmed
the significant impact of exposure to microplastics on feeding and
growth traits, and has highlighted a significant impact on fish behav-
iour and an important relationship between exposure to microplas-
tics, size and life stage of fish.
Among the investigated response variables, the one with the great-
est impact is feeding, followed by behaviour and growth. These re-
sults could be explained by the fact that the accumulation of ingested
microplastics in the digestive tract of fishes may lead to malnutrition
and eventual starvation (Boerger et al., 2010), and consequently
lower energy intake. This could mean less energy and resources
allocated to the fundamental physiological processes of growth and
reproduction (Marn et al., 2020). Yin et al. (2019) reported that, in
order to maintain normal functions under stressful conditions, black
rockfish exposed to polystyrene showed significant reduction of
available energy for growth through increased metabolic demands,
while a reduction in protein content was observed as well. The
presence of plastics pro- duced a negative scope for growth in crabs;
ammonia excretion and the metabolic costs of oxygen consumption
outweigh the energy obtained from food ingestion (Watts et al., 2015).
Moreover, plastics could affect ingestion or cause gastrointestinal
blockage (Avery-Gomm et al., 2012; Cole et al., 2015). Organisms
need to use internal reserves for their maintenance when plastics
are present in the environment, something that may result in
impairment of fundamental physiological processes. Fishes that
could count on a minor amount of energy may become less reactive
and slower at swimming. Moreover, lesions in organs such as the
liver and the intestine, due to microplastic ingestion, might result in an
abnormal fish swimming pattern (Yin et al., 2019).
Even when not ingested, microplastics can still have a nega-
tive impact on fish and their behaviour. For example, adherence
of microplastics to gills and skin may change oxygen consumption
and ion regulation causing respiratory stress, thus influencing be-
haviour (Abdel-Tawwab et al., 2019; W atts et al., 2016). Moreover,
locomotion impairment can have a significant impact on fish as a
predator and as a prey, influencing their survival (higher preda-
tion) or growth rate (feeding efficiency) and possibly leading to
reduced populations (Little & Finger, 1990). The altered prey–
predator relationships constitute an ecological concern, as
regards the preservation of the marine food web and community
struc- ture. Green et al. (2017) exposed sediment cores
containing a ben- thic community to microplastic particles and
found changes in the filtration rates of bivalves and differences in
associated infaunal invertebrate assemblages, thus highlighting
the potential effect of microplastics on marine ecologic
functioning and structure of sedimentary habitat.
SALERNO
Et
Subgroup analyses revealed different sensitivities of microplastic
exposure at the species level. This result was expected to a certain
extent. In fact, organisms belonging to different species have phys-
iological, anatomical and behavioural differences that make them
suitable for living in their environment but at the same time reacting
differently to the same stressor, such as microplastic pollution. This
could explain the differences among species responses to
microplas- tics (some have been highly impacted and others less,
while some displayed a positive effect size). However, these
differences are not found between groups during habitat and water
column habitat sub- group analyses; this leads us to think that
freshwater, marine or estu- arine species, or species adapted to life
in the water column or near the bottom, are equally vulnerable to
microplastics.
Life stage subgroup analyses highlighted significant differences
between development phases, suggesting that, depending on their
life stage, organisms may be more sensitive to microplastic pollu-
tion. Interestingly, results showed greater sensitivity in juveniles. We
infer the size of an organism is a key factor for interpreting these
results. It might be easier for juveniles to access a wider range of
microplastic sizes through ingestion. During the larval stage, in fact,
larvae can eat food (or microplastic) particles that are a bit smaller
than their mouth gaps. Slow development of the oral cavity of
Epinephelus coioides at an early stage created difficulties in feeding
the larvae with the right food (Kohno et al., 1997). Azfar Ismail et al.
(2019) found that larval mahseer hybrid started exogenous feeding
at 3 days after hatching as soon as its mouth began to open and
move (average total body length 4.80 mm); the study also indicated
that suitable prey size for the first feeding of the mahseer larvae was
111–173 μm in diameter. Thus, it is believed that larvae developing
slowly, with too small or not fully developed mouthparts, may be
unable to swallow microplastic items that are larger than their mouth
gaps and, therefore, are not exposed to specific ranges of micro-
plastic sizes. Based on this idea, we ran a meta-regression analysis,
relating the size of the organisms and the effect size. Results
showed a significant correlation between larval dimension and
effect size; the larger the size, the larger the negative effect size. In
line with our initial idea, it appears that, up to the juvenile phase, the
impact of microplastics depends on size at larval stage and size of
mouthpart, which means that the impact becomes increasingly
important with growth. Adults, on the other hand, do not seem to be
particularly sensitive to microplastics and this is consistent with the
findings of Foley et al. (2018). This main finding is in accordance
with differ- ences found when comparing the effect of microplastics
exposure on various taxonomic groups, that is juvenile stages of
echinoderms and mollusc invertebrates were less impacted
compared to juveniles of zooplankton and fishes (Foley et al., 2018).
In the course of our study, we also wondered whether the effects
of microplastics on organisms could vary depending on the intrinsic
characteristics of the microplastics or the conditions under which
fish encounter microplastic particles. Our analysis showed that
among the experimental conditions analysed, the time of exposure
to microplastics was relevant, suggesting that organisms exposed
to microplastics for long periods were the most vulnerable. Among
SALERNO
AL.
Et
shapes, fibres and fragment plastic particles were reported as hav-
ing a greater impact according to Pirsaheb et al. (2020), who found
that fibres and fragments with a rough surface (sharp edges)
caused more physical damage than spherical microplastics. The
analysis conducted on microplastic type suggested that there was
no spe- cific type of microplastic that affected organisms more than
others. Lei et al. (2018) who tested the toxic effects of five different
types of microplastics on zebrafish conclude that the toxicity of
microplas- tics is closely dependent on their size and concentration,
rather than their composition. Unfortunately, we did not have
sufficient case studies to test microplastic concentration, due to the
high heteroge- neity of methods used to report microplastic
concentrations (highly variable information from study to study),
precluding a comprehen- sive analysis of concentration effects. The
high heterogeneity of ex- perimental designs and methods used was
one of the more relevant issues encountered while performing this
meta-analysis, highlighting the need for future standardised
methods.
Moreover, some information was missing from several studies
such as, for example, the type of error presented in tables or figures,
or the sample size which was not always reported. We strongly rec -
ommend always including these details as well as the non-
significant results, that sometimes were not reported even in the
Supporting Information, to fully understand the impact of emerging
issues.
5 | CO NCL USIO NS
Evidence from our global meta-analysis confirmed that microplas-
tic pollution can compromise the fitness of fishes, which can affect
ecosystem functioning. Changes in growth rates, and development
of early life stage and behavioural patterns in fishes may have a
nega- tive effect on the structure and functions of the aquatic
ecosystem in the long term and consequently influence the ability of
these to provide ecosystem services and sustain human
communities. Fishes represent major sources of protein for entire
communities relying ex- clusively on fish. A decrease in fish
populations and the nutritional quality of individuals may have a
large impact not only on the human diet (and other predators too),
but also influence cultural traditions and the economies (from
coastal to global). Thus, we pinpoint that the effects of microplastic
exposure represent a major issue for practically all aquatic systems
on the planet, and our findings sup- port the scientific and public
concern over plastic pollution of aquatic ecosystems. Therefore, we
acknowledge the importance of echo- ing the scientific community's
call for more standardised reporting and evaluation methods for
microplastic densities and experiments (Bucci et al., 2020; Foley et
al., 2018), and recommend evaluation of bioaccumulation
(interaction between microplastics and contami- nants) and
biomagnification (capacity of microplastic particles per se as the
toxic micropollutant of interest) that may influence the per- formance
of organisms across the food web (Alava, 2020; Rochman et al.,
2013). Finally, our results underline the importance to focus on
functional and performance traits to support a trait-based indicator
development (Beauchard et al., 2017).
| 2653
ACKNOWLEDG EMENTS
This research was partially funded by the PRIN–MAHRES project
(Ministry of Italian Research; MUR) 2017MHHWBN_003 Linea C.
We thank L. Santangelo for her help on the literature review.
M.S. was supported by a research scholarship funded by
HARMONY Project Italy-Malta 2016 (grant C1-3.1-31) funded by the
Sicilian Region and Maltese Government. M.B. was supported by a
PhD research fellowship funded by the National Institute of
Oceanography and Applied Geophysics; M.C.M.'s research activity
was supported by the European Union's Horizon 2020 Research
and Innovation programme under the Marie Skłodowska-Curie
(grant agreement no. 835589, MIRROR Project). The authors wish
to rec- ognise the value of the “Meta-analysis in ecology, evolution
and en- vironmental science” course organised by PR Statistics and
delivered live (30 November 2020 to 4 December 2020) by Prof. Julia
Koricheva and Prof. Elena Kulinskaya, that facilitated the
understanding of data analysis to be integrated after the first round of
revision. We sincerely thank the three anonymous reviewers whose
critical reading resulted in inspiring comments that helped improve
and clarify this manuscript.
DATA AVAIL ABILIT Y STATEMENT
Data are available on request from the authors.
ORCID
Manuel Berlino https://orcid.org/0000-0003-0539-7345
M. Cristina Mangano https://orcid.org/0000-0001-6980-9834
Gianluca Sarà https://orcid.org/0000-0002-7658-5274
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SUPPORTING INFORMATION
Additional supporting information may be found online in the
Supporting Information section.
How to cite this article: Salerno M, Berlino M, Mangano MC,
Sarà G. Microplastics and the functional traits of fishes: A
global meta-analysis. Glob Change Biol. 2021;27:2645–2655.
https://doi.org/10.1111/gcb.15570
1 Supplementary Information for
2 M. Salerno, M. Berlino, M. C. Mangano and G. Sarà

3 Microplastics affect the fishes functional traits: insight from a global meta-analysis

5 Content
6 Supplementary text: Scoping exercise
7 Table S1 – S4
8 Figure S1 – S3
9 References list (from Table S3)
10
11 Scoping exercise

12 The first literature search was performed using a less complex and more general research string

13 (Search string #1, Table S1). The string was searched on the two main publication databases ISI Web

14 of Knowledge (Web of Science Core Collection package, Clarivate Analytics, 2019) and Scopus. The

15 search was performed without applying nor temporal neither spatial geographic scale restriction (to

16 ensure a full temporal and global scale coverage) final search date 20/05/2020. The search retrieved

17 a number of scientific papers larger than what we expected to obtain (Hits = 339; Table S1 Search

18 string #1), additionally when start screening the retrieved scientific articles we realized that a large

19 amount was mostly based on the simple observation (e.g. occurrence, chemical composition, structure

20 analysis), finding (e.g. sampling and isolation), extraction (e.g. comparison of microplastics

21 extraction protocols or tuning of novel approach) and characterisation of microplastics without

22 measuring fish traits response to microplastics (exclusion rate calculated over the 50 first hits was of

23 92%).

24 From that the decision to add to our search string another block of keywords to focus on the

25 observation type we were searching (“laboratory” OR “mesocosm*” OR “experiment*” OR

26 “treatment*”) that typically refer to a handling and measurement by researchers, aimed at increasing

27 the accuracy of our search (Search string #2, Table S1). This allows to avoid the inclusion of the large

28 number of studies reporting the microplastic presence occurrence in the field only with not associated

29 measured effects reported, or rather, to increase the accuracy of our search string and to

30 comprehensively reply to our main research question “What are the impacts of microplastics on the

31 functional traits of fish species?”. The new search run retrieved 219 hits (exclusion rate calculated

32 over the 50 first 50 hits was of 82% a reduction of 10% compared to the previous search string #1 as

33 proof of a higher representativeness of this latter search string #2). 24 scientific papers have been

34 manually added after reading the references list of several existing review on microplastics. After the

35 removal of duplicates papers (Hits = 208) have been subject to two runs of screening based on the
36 inclusions criteria and on the presence of the search string main elements (first level screening at

37 “Title and Abstract” reading, second screening “Full text” reading; Figure S1), a final number of 43

38 scientific papers was considered suitable for our meta-analysis work. Details of the studies included

39 in the meta-analysis (including k = number of case of studies) are reported into Table S2, while the

40 excluded studies are listed into Table S3.

41
42 Table S1 Search strings tested and final one used to retrieve the scientific paper used in the meta-analysis.
43 Notes: the wildcard asterisk (*) following a search key-word has been used allowing the search engine to
44 consider and accept the word variation in the search; quotation marks around key-word indicate the exact word
45 allowed in the search results; the number of records in the library after checking for duplicate, and before
46 performing the screening steps was 43.

Engine search HITS

Databases Scopus ISI WoK
TITLE-ABS-
Search fields Topic
KEY
Search string #1 TITLE-ABS-KEY(("microplastic*" OR "micro plastic*" 339 335
OR "micro-plastic*") AND ("trait*" OR "function*" OR
"response*" OR "measure*" OR "rate*" OR "Behaviour"
OR "Feeding" OR "Growth" OR "Health" OR "Hatching"
OR "Survival") AND ("*fish*"))

Search string #2 TITLE-ABS-KEY(("microplastic*" OR "micro plastic*" 219 217

OR "micro-plastic*") AND ("trait*" OR "function*" OR
"response*" OR "measure*" OR "rate*" OR "Behaviour"
OR "Feeding" OR "Growth" OR "Health" OR "Hatching"
OR "Survival") AND ("laboratory*" OR "mesocosm*"
OR "experiment*" OR "treatment*") AND ("*fish*"))

47
 48 Figure S1 Modified PRISMA (Preferred Reporting Items for Systematic Reviews and Meta‐Analysis) flow
49 diagram indicating the number of studies considered at each step (identified in vertical boxes on left) of the
50 literature search and meta‐analysis.
Identification

219 of records identified 24 of additional records

through database searching identified through other sources

208 of records after duplicates removed

Screening

208 of records screened 158 of records

excluded
Eligibility

50 of full-text articles 7 of full-text articles

assessed for eligibility excluded, with reasons

43 of studies included in
quantitative synthesis
(meta-analysis)
Included

51
52
53 Table S2 List of excluded studies.
54
Authors Title Year Source title Document type Reason for exclusion
Ahrendt, C., Perez-Venegas, Microplastic ingestion cause intestinal lesions in the 2020 Marine Pollution Article Abstract: histological
D. J., Urbina, M., Gonzalez, intertidal fish Girella laevifrons. Bulletin analyses
C., Echeveste, P., Aldana,
M., ... & Galbán-Malagón, C.
Avio, C. G., Pittura, L., Distribution and characterization of microplastic particles 2020 Environmental Article Abstract: observational
d’Errico, G., Abel, S., and textile microfibers in Adriatic food webs: General Pollution
Amorello, S., Marino, G., ... insights for biomonitoring strategies.
& Regoli, F.
Baechler, B. R., Stienbarger, Microplastic occurrence and effects in commercially 2020 Limnology and Review Abstract: review
C. D., Horn, D. A., Joseph, J., harvested North American finfish and shellfish: Current Oceanography Letters
Taylor, A. R., Granek, E. F., knowledge and future directions.
& Brander, S. M.
Barletta, M., Costa, M. F., & Ecology of microplastics contamination within food webs 2020 MethodsX Article Abstract: observational
Dantas, D. V. of estuarine and coastal ecosystems.
Batel, A., Baumann, L., Histological, enzymatic and chemical analyses of the 2020 Marine Pollution Article Title: histological analyses
Carteny, C. C., Cormier, B., potential effects of differently sized microplastic particles Bulletin
Keiter, S. H., & Braunbeck, upon long-term ingestion in zebrafish (Danio rerio).
T.
Binelli, A., Pietrelli, L., Di Hazard evaluation of plastic mixtures from four Italian 2020 Science of The Total Article Title: benthos
Vito, S., Coscia, L., subalpine great lakes on the basis of laboratory exposures Environment
Sighicelli, M., Della Torre, of zebra mussels.
C., ... & Magni, S.
Boyle, D., Catarino, A. I., Polyvinyl chloride (PVC) plastic fragments release Pb 2020 Environmental Article Abstract: gene expression
Clark, N. J., & Henry, T. B. additives that are bioavailable in zebrafish. Pollution analyses

Bringer, A., Thomas, H., High density polyethylene (HDPE) microplastics impair 2020 Environmental Article Title: benthos
Prunier, G., Dubillot, E., development and swimming activity of Pacific oyster D- Pollution
Bossut, N., Churlaud, C., ... larvae, Crassostrea gigas, depending on particle size.
& Cachot, J.
Duan, Z., Duan, X., Zhao, S., Barrier Function of Zebrafish Embryonic Chorions 2020 Journal of Hazardous Article Title: effects on embryon
Wang, X., Wang, J., Liu, Y., Against Microplastics and Nanoplastics and Its Impact on Materials
... & Wang, L. Embryo Development.
Elizalde-Velázquez, A.,
Carcano, A. M., Crago, J.,
Green, M. J., Shah, S. A., &
Cañas-Carrell, J. E.
Felten, V., Toumi, H.,
Masfaraud, J. F., Billoir, E.,
Camara, B. I., & Férard, J. F.
Ferreira, M., Thompson, J.,
Paris, A., Rohindra, D., &
Rico, C.
Fred-Ahmadu, O. H.,
Bhagwat, G., Oluyoye, I.,
Benson, N. U., Ayejuyo, O.
O., & Palanisami, T.
Gu, W., Liu, S., Chen, L.,
Liu, Y., Gu, C., Ren, H. Q.,
& Wu, B.
Translocation, trophic transfer, accumulation and 2020 Environmental Article Abstract: not related to
depuration of polystyrene microplastics in Daphnia Pollution functional traits
magna and Pimephales promelas.
Microplastics enhance Daphnia magna sensitivity to the 2020 Science of The Total Article Title: zooplankton
pyrethroid insecticide deltamethrin: Effects on life history Environment
traits.
Presence of microplastics in water, sediments and fish 2020 Marine Pollution Article Title: observational
species in an urban coastal environment of Fiji, a Pacific Bulletin
small island developing state.
Interaction of chemical contaminants with microplastics: 2020 Science of The Total Review Title: review
Principles and perspectives. Environment
Single-Cell RNA Sequencing Reveals Size-Dependent 2020 Environmental Science Article Title: analyses at cellular
Effects of Polystyrene Microplastics on Immune and & Technology and sub-cellular level
Secretory Cell Populations from Zebrafish Intestines.

Hoang, T. C., & Felix-Kim, Microplastic consumption and excretion by fathead 2020 Science of The Total Article Abstract: not related to
M. minnows (Pimephales promelas): Influence of particles Environment functional traits
size and body shape of fish.
Huuskonen, H., i Folguera, J. Do whitefish (Coregonus lavaretus) larvae show adaptive 2020 Environmental Article Abstract: not related to
S., Kortet, R., Akkanen, J., variation in the avoidance of microplastic ingestion? Pollution functional traits
Vainikka, A., Janhunen, M.,
& Kekäläinen, J.
Iheanacho, S. C., & Odo, G. Neurotoxicity, oxidative stress biomarkers and 2020 Comparative Article Title: analyses at cellular
E. haematological responses in African catfish (Clarias Biochemistry and and sub-cellular level
gariepinus) exposed to polyvinyl chloride microparticles. Physiology Part C:
Toxicology &
Pharmacology
Jacob, H., Besson, M., Effects of Virgin Micro-and Nanoplastics on Fish: Trends, 2020 Environmental Science Review Abstract: review
Swarzenski, P. W., Lecchini, Meta-Analysis, and Perspectives. & Technology
D., & Metian, M.
Keisling, C., Harris, R. D., Low concentrations and low spatial variability of marine 2020 Marine pollution Article Title: benthos
Blaze, J., Coffin, J., & Byers, microplastics in oysters (Crassostrea virginica) in a rural bulletin
J. E. Georgia estuary.
Li, C., Busquets, R., & Assessment of microplastics in freshwater systems: A 2020 Science of The Total Review Title: review
Campos, L. C. review. Environment
Liu, Y., Zhang, J., Cai, C.,
He, Y., Chen, L., Xiong, X.,
... & Liu, W.
Lu, S., Qiu, R., Hu, J., Li, X.,
Chen, Y., Zhang, X., ... &
He, D.
Mbachu, O., Jenkins, G.,
Pratt, C., & Kaparaju, P.
Mbedzi, R., Dalu, T.,
Wasserman, R. J.,
Murungweni, F., & Cuthbert,
R. N.
Naidoo, T., Thompson, R. C.,
& Rajkaran, A.
Nan, B., Su, L., Kellar, C.,
Craig, N. J., Keough, M. J.,
& Pettigrove, V.
Nanninga, G. B., Scott, A., &
Manica, A.
Sarasamma, S., Audira, G.,
Siregar, P., Malhotra, N., Lai,
Y. H., Liang, S. T., ... &
Hsiao, C. D.
Sierra, I., Chialanza, M. R.,
Faccio, R., Carrizo, D.,
Fornaro, L., & Pérez-Parada,
A.
Talley, T. S., Venuti, N., &
Whelan, R.
Tang, S., Lin, L., Wang, X.,
Feng, A., & Yu, A.
Tang, Y., Rong, J., Guan, X.,
Zha, S., Shi, W., Han, Y., ...
& Liu, G.
Occurrence and characteristics of microplastics in the 2020 Environmental Article Title: enviromental
Haihe River: An investigation of a seagoing river flowing Pollution pollution
through a megacity in northern China.
Prevalence of microplastics in animal-based traditional 2020 Science of The Total Article Title: terrestrial
medicinal materials: Widespread pollution in terrestrial Environment environments
environments.
A New Contaminant Superhighway? A Review of 2020 Water, Air, & Soil Review Title: review
Sources, Measurement Techniques and Fate of Pollution
Atmospheric Microplastics.
Functional response quantifies microplastic uptake by a 2020 Science of The Total Article Abstract: not related to
widespread African fish species. Environment functional traits
Quantification and characterisation of microplastics 2020 Environmental Article Title: observational
ingested by selected juvenile fish species associated with Pollution
mangroves in KwaZulu-Natal, South Africa.
Identification of microplastics in surface water and 2020 Environmental Article Title: freshwater shrimp
Australian freshwater shrimp Paratya australiensis in Pollution
Victoria, Australia.
Microplastic ingestion rates are phenotype-dependent in 2020 Environmental Article Full text: extraction data not
juvenile anemonefish. Pollution possible
Nanoplastics Cause Neurobehavioral Impairments, 2020 International Journal of Article Title: nanoplastics
Reproductive and Oxidative Damages, and Biomarker Molecular Sciences
Responses in Zebrafish: Throwing up Alarms of Wide
Spread Health Risk of Exposure.
Identification of microplastics in wastewater samples by 2020 Environmental Science Article Title: Identification of MPs
means of polarized light optical microscopy. and Pollution Research in wastewater
Natural history matters: Plastics in estuarine fish and 2020 Plos one Article Abstract: observational
sediments at the mouth of an urban watershed.
Pb (II) uptake onto nylon microplastics: Interaction 2020 Journal of Hazardous Article Title: contaminant
mechanism and adsorption performance. Materials
Immunotoxicity of microplastics and two persistent 2020 Environmental Article Title: benthos
organic pollutants alone or in combination to a bivalve Pollution
species.
Thomas, M., Jon, B., Craig,
S., Edward, R., Ruth, H.,
John, B., ... & Matthew, S.
van der Hal, N., Yeruham, E.,
Shukis, D., Rilov, G.,
Astrahan, P., & Angel, D. L.
Wang, W., Ge, J., & Yu, X.
Wang, Y. L., Lee, Y. H.,
Chiu, I. J., Lin, Y. F., &
Chiu, H. W.
Xie, X., Deng, T., Duan, J.,
Xie, J., Yuan, J., & Chen, M.
Yan, W., Hamid, N., Deng,
S., Jia, P. P., & Pei, D. S.
Yao, L., Hui, L., Yang, Z.,
Chen, X., & Xiao, A.
Yu, Y., Ma, R., Qu, H., Zuo,
Y., Yu, Z., Hu, G., ... & Yu,
G.
Zeytin, S., Wagner, G.,
Mackay-Roberts, N., Gerdts,
G., Schuirmann, E.,
Klockmann, S., & Slater, M.
Andrady, A. L., Pandey, K.
K., & Heikkilä, A. M.
Arossa, S., Martin, C.,
Rossbach, S., & Duarte, C.
M.
Banaee, M., Soltanian, S.,
Sureda, A., Gholamhosseini,
A., Haghi, B. N., Akhlaghi,
M., & Derikvandy, A.
The world is your oyster: low-dose, long-term 2020 Heliyon Article Title: benthos
microplastic exposure of juvenile oysters.
Uptake and incorporation of PCBs by eastern 2020 Marine Pollution Article Title: contaminant
Mediterranean rabbitfish that consumed microplastics. Bulletin
Bioavailability and toxicity of microplastics to fish 2020 Ecotoxicology and Review Title: review
species: A review. environmental safety
Potent impact of plastic nanomaterials and micromaterials 2020 International Journal of Review Title: review
on the food chain and human health. Molecular Sciences
Exposure to polystyrene microplastics causes 2020 Ecotoxicology and Article Abstract: terrestrial animals
reproductive toxicity through oxidative stress and Environmental Safety
activation of the p38 MAPK signaling pathway.
Individual and combined toxicogenetic effects of 2020 Journal of Hazardous Article Full text: insufficient data
microplastics and heavy metals (Cd, Pb, and Zn) perturb Materials
gut microbiota homeostasis and gonadal development in
marine medaka (Oryzias melastigma).
Freshwater microplastics pollution: Detecting and 2020 Chemosphere Review Title: review
visualizing emerging trends based on Citespace II.
Enhanced adsorption of tetrabromobisphenol a (TBBPA) 2020 Chemosphere Article Full text: not related to
on cosmetic-derived plastic microbeads and combined functional traits
effects on zebrafish.
Quantifying microplastic translocation from feed to the 2020 Marine Pollution Article Title: not related to
fillet in European sea bass Dicentrarchus labrax. Bulletin functional traits
Interactive effects of solar UV radiation and climate 2019 Photochemical & Article Title: not related to the
change on material damage. Photobiological effect of microplastics on
Sciences fish
Microplastic removal by Red Sea giant clam (Tridacna 2019 Environmental pollution Article Title: benthos
maxima).
Evaluation of single and combined effects of cadmium and 2019 Chemosphere Article Title: biochemical and
micro-plastic particles on biochemical and immunological immunological analyses
parameters of common carp (Cyprinus carpio).
Bayo, J., Rojo, D., & Olmos,
S.
Botterell, Z. L., Beaumont,
N., Dorrington, T., Steinke,
M., Thompson, R. C., &
Lindeque, P. K.
Bussolaro, D., Wright, S. L.,
Schnell, S., Schirmer, K.,
Bury, N. R., & Arlt, V. M.
Carrasco, A., Pulgar, J.,
Quintanilla-Ahumada, D.,
Perez-Venegas, D., Quijón,
P. A., & Duarte, C.
Cho, Y., Shim, W. J., Jang,
M., Han, G. M., & Hong, S.
H.
Coffin, S., Lee, I., Gan, J., &
Schlenk, D.
Collard, F., Gasperi, J.,
Gabrielsen, G. W., & Tassin,
B.
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Bahar, B. B.
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Caldeira, K.
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Gelatt, T., Ream, R., Baker,
J. D., Faulhaber, K., &
Lerner, D. T.
Fangzhu, W., Jiangning, Z.,
Xiaoqun, X., Youji, W.,
Qiang, L., Xudan, X., & Wei,
H.
Abundance, morphology and chemical composition of 2019 Environmental Article Title: microplastics in
microplastics in sand and sediments from a protected Pollution sediment
coastal area: The Mar Menor lagoon (SE Spain).
Bioavailability and effects of microplastics on marine 2019 Environmental Review Title: zooplankton
zooplankton: A review. Pollution
Co-exposure to polystyrene plastic beads and polycyclic 2019 Environmental pollution Article Title: analyses at cellular
aromatic hydrocarbon contaminants in fish gill (RTgill- and sub-cellular level
W1) and intestinal (RTgutGC) epithelial cells derived
from rainbow trout (Oncorhynchus mykiss).
The influence of microplastics pollution on the feeding 2019 Marine pollution Article Title: sandy beach
behavior of a prominent sandy beach amphipod, bulletin amphipod
Orchestoidea tuberculata (Nicolet, 1849).
Abundance and characteristics of microplastics in market 2019 Environmental pollution Article Title: benthos
bivalves from South Korea.
Simulated digestion of polystyrene foam enhances 2019 Environmental pollution Article Title: simulated digestion
desorption of diethylhexyl phthalate (DEHP) and In vitro process in vitro
estrogenic activity in a size-dependent manner.
Plastic particle ingestion by wild freshwater fish: a critical 2019 Environmental science Review Title: review
review. & technology
Analysis of Microplastic Content in Baronang Fish 2019 Indian Journal of Public Article Abstract: observational
(Siganus sp) and Kakap Fish (Lutjanus sp) in the Coastal Health Research &
Area of Bangkala Subdistrict, Jeneponto Regency. Development
Response of bleached and symbiotic sea anemones to 2019 Environmental pollution Article Title: sea anemones
plastic microfiber exposure.
Evaluating exposure of northern fur seals, Callorhinus 2019 Marine pollution Article Title: northern fur seals
ursinus, to microplastic pollution through fecal analysis. bulletin
Status of marine microplastic pollution and its 2019 海洋学报 Article Full text: japanese language
ecotoxicological effects on marine fish.
Hanachi, P., Karbalaei, S.,
Walker, T. R., Cole, M., &
Hosseini, S. V.
Heinrich, P., & Braunbeck,
T.
Henry, B., Laitala, K., &
Klepp, I. G.
Ho, L. T., & Goethals, P. L. .
Hunsucker, K., Melikov, A.,
Gilligan, M., Gardner, H.,
Weaver, R., & Swain, G.
Jaikumar, G., Brun, N. R.,
Vijver, M. G., & Bosker, T.
Kokalj, A. J., Kuehnel, D.,
Puntar, B., Gotvajn, A. Ž., &
Kalčikova, G.
Leads, R. R., Burnett, K. G.,
& Weinstein, J. E.
Lee, H., Lee, H. J., & Kwon,
J. H.
Liu, Z., Yu, P., Cai, M., Wu,
D., Zhang, M., Chen, M., &
Zhao, Y.
Mak, C. W., Yeung, K. C. F.,
& Chan, K. M.
Markic, A., Gaertner, J. C.,
Gaertner-Mazouni, N., &
Koelmans, A. A.
Abundance and properties of microplastics found in 2019 Environmental Science Article Abstract: not related to
commercial fish meal and cultured common carp and Pollution Research functional traits
(Cyprinus carpio).
Microplastic testing in vitro: Realistic loading of 2019 Toxicology in Vitro Article Title: testing in vitro
pollutants, surfactant-free solid surface-dosing and
bioanalytical detection using a sensitivity-optimized
EROD assay.
Microfibres from apparel and home textiles: prospects for 2019 Science of the Total Article Title: enviromental
including microplastics in environmental sustainability Environment pollution
assessment.
Opportunities and challenges for the sustainability of lakes 2019 Water Review Title: sustainability of lakes
and reservoirs in relation to the Sustainable Development and reservoirs
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Mineral Accretion: An Environmentally Alternative to 2019 OCEANS 2019 Article Title: benthos
Plastic for Oyster Restoration. MTS/IEEE SEATTLE
Reproductive toxicity of primary and secondary 2019 Environmental pollution Article Title: cladocerans
microplastics to three cladocerans during chronic
exposure.
An exploratory ecotoxicity study of primary microplastics 2019 Environmental Article Full text: insufficient data
versus aged in natural waters and wastewaters. Pollution
The Effect of Microplastic Ingestion on Survival of the 2019 Environmental Article Title: Grass Shrimp
Grass Shrimp Palaemonetes pugio (Holthuis, 1949) toxicology and
Challenged with Vibrio campbellii. chemistry
Estimating microplastic-bound intake of hydrophobic 2019 Science of the Total Article Title: artificial gut fluid
organic chemicals by fish using measured desorption rates Environment
to artificial gut fluid.
Effects of microplastics on the innate immunity and 2019 Science of the Total Article Title: chinese mitten crab
intestinal microflora of juvenile Eriocheir sinensis. Environment
Acute toxic effects of polyethylene microplastic on adult 2019 Ecotoxicology and Article Full text: insufficient data
zebrafish. environmental safety
Plastic ingestion by marine fish in the wild. 2019 Critical Reviews in Review Abstract: review
Environmental Science
and Technology
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Hester, M. A., Arthur, C., &
Rutherford, N.

Miranda, T., Vieira, L. R., &
Guilhermino, L.
Mishra, S., charan Rath, C.,
& Das, A. P.
Peixoto, D., Amorim, J.,
Pinheiro, C., Oliva-Teles, L.,
Varó, I., de Medeiros Rocha,
R., & Vieira, M. N.
Porter, A., Smith, K. E., &
Lewis, C.
Qiao, R., Sheng, C., Lu, Y.,
Zhang, Y., Ren, H., &
Lemos, B.
Qu, H., Ma, R., Wang, B.,
Yang, J., Duan, L., & Yu, G.
Neurotoxicity, Behavior, and Lethal Effects of Cadmium, 2019 International journal of Article Abstract: contaminant?
Microplastics, and Their Mixtures on Pomatoschistus environmental research
microps Juveniles from Two Wild Populations Exposed and public health
under Laboratory Conditions―Implications to
Environmental and Human Risk Assessment.
Marine microfiber pollution: a review on present status 2019 Marine pollution Review Title: review
and future challenges. bulletin
Uptake and effects of different concentrations of spherical 2019 Ecotoxicology and Article Title: Artemia
polymer microparticles on Artemia franciscana. environmental safety
The sea urchin Paracentrotus lividus as a bioeroder of 2019 Science of the Total Article Title: benthos
plastic. Environment
Microplastics induce intestinal inflammation, oxidative 2019 Science of the Total Article Abstract: analyses at
stress, and disorders of metabolome and microbiome in Environment cellular and sub-cellular
zebrafish. level
Enantiospecific toxicity, distribution and bioaccumulation 2019 Journal of hazardous Article Title: contaminat
of chiral antidepressant venlafaxine and its metabolite in materials
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Schmidt, T. C., & Schram, J.
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Parsley, L. M., Wilcox, C., from a plastic feeding experiment. Environment
Hardesty, B. D., Gilardi, K.,
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E., & Gutow, L. straightforward approach of the Atlantic ditch shrimp Pollution
Palaemon varians.
Severini, M. D. F., Villagran, Microplastics in oysters (Crassostrea gigas) and water at 2019 Regional Studies in Article Title: benthos
D. M., Buzzi, N. S., & Sartor, the Bahía Blanca Estuary (Southwestern Atlantic): An Marine Science
G. C. emerging issue of global concern.
Syakti, A. D., Jaya, J. V.,
Rahman, A., Hidayati, N. V.,
Raza'i, T. S., Idris, F., ... &
Chou, L. M.
Uriarte, A., Johnstone, C.,
Laiz-Carrión, R., García, A.,
Llopiz, J. K., Shiroza, A., ...
& Alemany, F.
Wang, X., Jiang, X. R., Wu,
F., Ma, Y., Che, X., Chen,
X., ... & Chen, G. Q.
Wang, Y., Mao, Z., Zhang,
M., Ding, G., Sun, J., Du, M.,
... & Wang, J.
Watkins, L., Sullivan, P. J., &
Walter, M. T.
Windsor, F. M., Tilley, R.
M., Tyler, C. R., & Ormerod,
S. J.
Winkler, A., Santo, N.,
Ortenzi, M. A., Bolzoni, E.,
Bacchetta, R., & Tremolada,
P.
Amorim, M. J., Lin, S.,
Schlich, K., Navas, J. M.,
Brunelli, A., Neubauer, N., ...
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Ašmonaitė, G., Larsson, K.,
Undeland, I., Sturve, J., &
Carney Almroth, B.
Barboza, L. G. A., Vieira, L.
R., Branco, V., Figueiredo,
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microplastics.
Evidence of density-dependent cannibalism in the diet of 2019 Fisheries Research Article Abstract: observational
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Microplastic ingestion by riverine macroinvertebrates. 2019 Science of the Total Article Title: macroinvertebrates
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Environmental impacts by fragments released from 2018 Environmental science Article Title: nanoplastics
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Size matters: ingestion of relatively large microplastics 2018 Environmental science Article Abstract: not related to
contaminated with environmental pollutants posed little & technology functional traits
risk for fish health and fillet quality.
Microplastics cause neurotoxicity, oxidative damage and 2018 Aquatic Toxicology Article Abstract: analyses at
energy-related changes and interact with the cellular and sub-cellular
bioaccumulation of mercury in the European seabass, level
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J., Cormier, B., Cousin, X.,
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Miller, M. E., Kroon, F. J., & Recovering microplastics from marine samples: A review 2017 Marine pollution Review Title: review
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55
56
57 Table S3 Details of the studies included in the meta-analysis (k = number of case of studies).

Author Species Trait k

Duan et al., 2020 Danio rerio Health 2
Development 20
Fecundity 12
Growth 12
Hu et al., 2020 Oryzias latipes
Hatching 6
Health 18
Survival 6
Behaviour 39
Development 3
Growth 3
Le Bihanic et al., 2020 Oryzias melastigma
Hatching 2
Health 3
Survival 2
Growth 6
Hatching 3
Li et al., 2020 Oryzias melastigma
Health 18
Survival 3
Behaviour 10
Development 110
Malafaia et al., 2020 Danio rerio
Hatching 13
Health 10
Schmieg et al., 2020 Salmo trutta Growth 1
Xia et al., 2020 Cyprinus carpio Growth 3
Growth 4
Zhao et al., 2020 Danio rerio
Health 2
Zhu et al., 2020 Oryzias latipes Fecundity 6
Fecundity 12
Chisada et al., 2019 Oryzias latipes
Growth 12
Fecundity 2
Growth 2
Cong et al., 2019 Oryzias melastigma
Hatching 1
Survival 1
Behaviour 3
Cormier et al., 2019 Danio rerio Growth 1
Hatching 4
Growth 14
Jinhui et al., 2019 Hippocampus kuda Health 7
Survival 1
Kim et al., 2019 Danio rerio Behaviour 25
Limonta et al., 2019 Danio rerio Behaviour 4
Miranda et al., 2019 Pomatoschistus microps Feeding 2
Naidoo & Glassom, 2019 Ambassis dussumieri Growth 9
Behaviour 6
Development 1
Pannetier et al., 2019 Oryzias latipes
Growth 2
Survival 1
Behaviour 12
Qiang & Cheng, 2019 Danio rerio Growth 2
Hatching 6
Growth 6
Qiao et al., 2019 Danio rerio
Health 4
Fecundity 5
Growth 3
Wang et al., 2019 Oryzias melastigma
Hatching 2
Health 33
Behaviour 9
Yin et al. 2019 Sebastes schlegelii
Health 2
Barboza et al., 2018 Dicentrarchus labrax Behaviour 2
Choi et al., 2018 Cyprinodon variegatus Behaviour 16
Behaviour 10
Critchell & Hoogenboom, 2018 Acanthochromis polyacanthus Growth 33
Health 12
Behaviour 1
Guven et al., 2018 Lates calcarifer
Feeding 1
Growth 6
Jabeen et al., 2018 Carassius auratus
Health 3
Jin et al., 2018 Danio rerio Health 2
Growth 6
Hatching 4
LeMoine et al., 2018 Danio rerio
Health 9
Survival 1
Feeding 12
Malinich et al., 2018 Pimephales promelas
Growth 7
Growth 2
Wen et al., 2018 Symphysodon aequifasciatus
Survival 2
Behaviour 1
Yin et al., 2018 Sebastes schlegelii Feeding 1
Health 1
Behaviour 6
Chen et al., 2017 Danio rerio
Growth 1
Espinosa et al., 2017 Sparus aurata Growth 8
Growth 12
Karami et al., 2017 Danio rerio
Health 6
 Feeding 4
Rochman et al., 2017 Acipenser transmontanus
Health 4
Ferreira et al., 2016 Pomatoschistus microps Feeding 2
Feeding 2
Fonte et al., 2016 Pomatoschistus microps
Growth 4
Behavior 22
Lönnstedt & Eklöv, 2016 Perca fluviatilis Growth 2
Hatching 1
Growth 12
Peda et al., 2016 Dicentrarchus labrax
Health 6
de Sá et al., 2015 Pomatoschistus microps Feeding 12
Luís et al., 2015 Pomatoschistus microps Feeding 2
Growth 4
Mazurais et al., 2015 Dicentrarchus labrax
Survival 1
58
59 Figure S2 Forest plot of the (a) “microplastic type” and (b) “microplastic shape” subgroups effect-size.
60 Analysis conducted with mixed-effects model, using the rma.mv function of the metaphor package in R,
61 including study Id and functional trait as random factor. Black boxes represent the Hedges’g (g) value and the
62 horizontal lines represent the 95% CI for each g value; Qm =omnibus test of moderators from the model; k =
63 number of study cases; level of statistical significance: p<0.01*, p<0.05*.
64
65
a)
66
67
68
69
70
71
72
73
74
75
76
77
78
79
80
81
82 b)
83
84
85
86
87
88
89
90
91 Figure S3 Forest plot of the (a) “days of exposure” and (b) “microplastic size” subgroups effect-size. Analysis
92 conducted with mixed-effects model, using the rma.mv function of the metaphor package in R, including study
93 Id and functional trait as random factor. Black boxes represent the Hedges’g (g) value and the horizontal lines
94 represent the 95% CI for each g value; Qm =omnibus test of moderators from the model; k = number of study
95 cases; level of statistical significance: p<0.001 ***, p<0.01**, p<0.05*.
96
97
a)
98
99
100
101
102
103
104
105
106
107
108
109
110
111 b)
112
113
114
115 Table S4 Summary of sensitivity analyses and publication bias outcomes. Random-effect model (before / after) sensitivity analysis results (n = number of case
116 studies, g = Hedges’ g, CI = 95% Confidence Interval). Potential publication bias z- and p-values reported for the intercept of the model. Outliers values, n = number
117 of outliers detected; “Change” column indicates whether outcome of the analysis was significantly different after removing potential outliers.

Random-effects model (before) Potential publication bias Outliers Random-effetcs model (after)
Effect size metric
n g ± 95% CI z-value p-value n n g ± 95% CI Change
Effects on functional trait of fish
Behavior 178 -0.4724 0.4568 0.2112 0.8327 12 166 -0.3556 0.3206 No
Development 134 -0.0384 0.1947 2.79925 0.0052 0 134 -0.0384 0.1947 No
Fecundity 38 -0.4893 0.5553 4.5394 <0.001 0 38 -0.4893 0.5553 No
Feeding 39 -0.5141 0.6599 1.3501 0.177 0 39 -0.5141 0.6599 No
Growth 192 -0.4112 0.3844 5.7726 <0.001 14 178 -0.2242 0.232 Yes
Hatching 47 -0.2937 0.4235 0.8762 0.3809 5 42 -0.0997 0.3956 No
Health 148 -0.084 0.4401 5.0367 <0.001 6 142 -0.0564 0.4059 No
Survival 19 -0.2005 0.5229 -3.4806 0.0005 1 18 -0.3251 0.5125 No
Effects per habitat
Marine 120 -0.4691 0.8669 4.8363 <.0001 16 104 -0.1529 0.5915 No
Freshwater 565 -0.2907 0.3611 6.2203 <.0001 18 547 -0.2312 0.1813 Yes
Estuarine 110 -0.3671 0.2792 3.2792 0.001 3 107 -0.3694 0.275 No
Effects per water column habitat
Benthopelagic 644 -0.3492 0.333 6.5689 <.0001 23 621 -0.282 0.1565 Yes
Demersal 116 -0.4384 0.4717 3.7105 0.0002 11 105 -0.2744 0.3634 Yes
Pelagic 35 0.1677 0.464 -0.4024 0.6874 3 32 0.1467 0.5108 No
Effects per life stage
Embryos 119 -0.2959 0.4072 2.7776 0.0055 7 112 -0.2729 0.2823 Yes
Larvae 324 -0.4005 0.4558 5.7247 <.0001 12 312 -0.2173 0.2026 Yes
Juvenile 189 -0.5246 0.3429 4.9027 <.0001 16 173 -0.3982 0.2527 No
Adult 163 -0.0365 0.2368 -1.4871 0.137 2 161 -0.0292 0.3962 No
Effects per species
Acanthochromis polyacanthus 60 -0.1279 0.3888 2.009 0.0445 5 55 -0.2 0.1783 No
Acipenser transmontanus 8 -0.1532 1.5322 3.4957 0.0005 0 8 -0.1532 1.5322 No
 Ambassis dussumieri 9 -0.3652 0.103 2.2706 0.0232 0 9 -0.3652 0.103 No
Carassius auratus 9 -0.214 0.2398 1.4312 0.1524 0 9 -0.214 0.2398 No
Cyprinodon variegatus 16 -0.5572 0.2524 2.5254 0.0116 0 16 -0.5572 0.2524 No
Cyprinus carpio 12 -4.113 0.512 1.4793 0.1391 0 12 -4.113 0.512 No
Danio rerio 270 -0.0772 0.211 0.8744 0.3819 5 265 -0.0851 0.1933 No
Dicentrarchus labrax 28 0.1838 0.7362 0.8747 0.3818 2 26 0.3867 0.3777 Yes
Hippocampus kuda 23 -0.5368 0.7718 2.2205 0.0264 1 22 -0.5038 0.7638 No
Oryzias latipes 114 -0.1709 0.2366 1.5395 0.1237 0 114 -0.1709 0.2366 No
Oryzias melastigma 136 -0.3291 0.4209 2.0527 0.0401 4 132 -0.2445 0.4463 No
Perca fluviatilis 28 -1.2122 1.462 -0.3348 0.7378 2 26 -1.234 1.4126 Yes
Pimephales promelas 19 0.176 0.2196 -0.3492 0.7269 0 19 0.176 0.2196 No
Pomatoschistus microps 24 -0.5299 0.5596 2.2077 0.0273 0 24 -0.5299 0.5596 No
Sebastes schlegelii 24 -1.8754 1.4726 2.0371 0.0416 3 21 -2.0041 1.1478 Yes
Sparus aurata 8 0.5725 0.4576 -1.9067 0.0566 0 8 0.5725 0.4576 No
Symphysodon aequifasciatus 4 -0.23 0.9365 2.3937 0.0167 0 4 -0.23 0.9365 No
118
119
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