Environmental Pollution 261 (2020) 114089

Contents lists available at ScienceDirect

Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

Microplastics in aquatic environments: Toxicity to trigger ecological

consequences*
Hui Ma a, b, Shengyan Pu a, c, d, *, Shibin Liu a, Yingchen Bai c, Sandip Mandal a,
Baoshan Xing d
a
State Key Laboratory of Geohazard Prevention and Geoenvironment Protection (Chengdu University of Technology), 1#, Dongsanlu, Erxianqiao, Chengdu
610059, Sichuan, PR China
b
Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej, 401871, Frederiksberg, Denmark
c
State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100012, PR China
d
Stockbridge School of Agriculture, University of Massachusetts, Amherst, MA 01003, United States

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

Article history: The prevalence of microplastic debris in aquatic ecosystems as a result of anthropogenic activity has
Received 18 September 2019 received worldwide attention. Although extensive research has reported ubiquitous and directly adverse
Received in revised form effects on organisms, only a few published studies have proposed the long-term ecological consequences.
20 January 2020
The research in this field still lacks a systematic overview of the toxic effects of microplastics and a
Accepted 27 January 2020
coherent understanding of the potential ecological consequences. Here, we draw upon cross-disciplinary
Available online 1 February 2020
scientific research from recent decades to 1) seek to understand the correlation between the responses of
organisms to microplastics and the potential ecological disturbances, 2) summarize the potential
Keywords:
Microplastics
ecological consequences triggered by microplastics in aquatic environments, and 3) discuss the barriers
Toxic effects to the understanding of microplastic toxicology. In this paper, the physiochemical characteristics and
Aquatic environment dynamic distribution of microplastics were related to the toxicological concerns about microplastic
Ecotoxicology bioavailability and environmental perturbation. The extent of the ecological disturbances depends on
how the ecotoxicity of microplastics is transferred and proliferated throughout an aquatic environment.
Microplastics are prevalent; they interfere with nutrient productivity and cycling, cause physiological
stress in organisms (e.g., behavioral alterations, immune responses, abnormal metabolism, and changes
to energy budgets), and threaten the ecosystem composition and stability. By integrating the linkages
among the toxicities that range from the erosion of individual species to the defective development of
biological communities to the collapse of the ecosystem functioning, this review provides a bottom-up
framework for future research to address the mechanisms underlying the toxicity of microplastics in
aquatic environments and the substantial ecological consequences.
© 2020 Elsevier Ltd. All rights reserved.

1. Introduction production has been estimated to reach 33 billion tons by 2050

Plastic has become a major commodity in the modern world on
an unprecedented global scale, penetrating basically every aspect of
our lives. The plastic industry expands annually, but the con-
sumption needs have not appeared to decrease. The total plastic
* not only that the small plastic particles from cosmetics, clothing
This paper has been recommended for acceptance by Da Chen.
* Corresponding author. State Key Laboratory of Geohazard Prevention and
Geoenvironment Protection (Chengdu University of Technology), Chengdu 610059,
PR China.
E-mail addresses: pushengyan@gmail.com, pushengyan13@cdut.cn,
pushengyan13@cdut.edu.cn (S. Pu).
(Olympic, 2013). Because plastic is a persistent synthetic polymer,
scientists started to question where all the discharged plastic debris
had gone (Thompson et al., 2004). Microplastics, which have been
reported sporadically since as early as the 1970s, are now believed
to be the predominant form of discharged plastic waste (Thompson
et al., 2004) and have generated considerable research interest
since 2004 (Rochman, 2018). The disappearance of plastics suggests
and other industrial manufacturing is entering into the aquatic
environment directly (as primary microplastics), but also that the
abundant microplastics are generated from the breakdown of large
plastic debris in the form of plastic fragments, fibers, and granules

https://doi.org/10.1016/j.envpol.2020.114089
0269-7491/© 2020 Elsevier Ltd. All rights reserved.
2 H. Ma et al. / Environmental Pollution 261 (2020) 114089
(as secondary microplastics) (Hidalgo-Ruz et al., 2012; Gonza
lez-
Pleiter et al., 2019). The recognition of microplastics as a globe
issue was raised from the detection of microplastics worldwide (Yu
et al., 2018a; Alimba and Faggio, 2019). Efforts have been made to
develop advanced sampling and analytical techniques with higher
accuracies in the wake of the increased research (Hidalgo-Ruz et al.,
2012; Strungaru, 2019; Chae and An, 2017). After the development
of these techniques, signs of stress were observed in organisms as a
€la
result of microplastics (Betts, 2008; Seta € et al., 2014; Proki

c, 2019).
Because of their small size and ubiquity, the microplastic particles
that spreaded in aquatic (Horton et al., 2017; Guzzetti et al., 2018),
terrestrial (Lwanga et al., 2016) and atmospheric (Dris et al., 2015;
Allen et al., 2019) environments have high bioavailability for
different species. The existence of microplastics has been found in
the guts of benthic invertebrates, fish (Savoca et al., 2019), and
larger mammals (Besseling et al., 2015) from different trophic
levels, and the ingested microplastics are transferred throughout
the food web, driving increasing concerns about the threats to
aquatic biota (Betts, 2008; Wright et al., 2013a). Both direct and
indirect evidence for the adverse effect of microplastics have been
found as a result of the interference with fecundity, mortality and
the dosage-effect relationship with physiological stress, including
behavioral alterations (Gambardella et al., 2017), immune re-
sponses (Veneman et al., 2017), abnormal metabolism (Jovanovic,
2017), and changes in energy budgets (Wright et al., 2013b).
We present this particular review because, whereas the negative
effect of microplastics on organisms and the environment have
been widely reported, the potential indirect impacts on the
ecosystem have received less attention, and few published results
have proposed long-term ecological consequences. However, the
question of whether the interference of microplastics is truly
harmful to the environment has hardly been addressed due to the
ambiguous results obtained from nonstandardized research
methods and the complexity of aquatic ecosystems (Hermsen et al.,
2017). A comprehensive comparison of the scattered results would
be beneficial for developing a sound and overarching framework
for an improved understanding of microplastics as an anthropo-
genic change in this new epoch. In this review, the most discussed
physiochemical characteristics were summarized from the
perspective of why the widely used plastics become toxic to the
aquatic environments in the form of microplastics. By systemically
summarizing the diverse toxicological effects of microplastics, the
links between the superficial phenomena and the in-depth toxi-
cological mechanisms were established to advance the knowledge
of the potential long-lasting ecological threats to the aquatic
ecosystem, providing a comprehensive framework and guidance
for future research. In addition, the most recent research gives
recommendations for the definition of microplastics (Hartmann
et al., 2019), but considering the diverse methods from the
studies in last decade, this review chose the most frequently used
definition to encompass the largest range of microplastics study,
which are the plastic particles under the size of 5000 mm, without
further differentiation of specific textures, shapes or compositions
(Moore, 2008; Arthur et al., 2009).
2. Clues from the features of microplastics: bioavailability
and toxicity are determined by the physicochemical
properties
In toxicological studies, the physicochemical properties of
microplastics are used to be provided as the fundamental infor-
mation, regardless of the research focus. However, the inherent
nature of microplastics is also related to their bioavailability and
toxicity in aquatic environments. Therefore, instead of describing
the physiochemical properties in detail, efforts will be made in this
review to reveal the influence on the ingestion preferences, bio-
logical responses of different species and the profound ecological
implications.
2.1. Physical property
Bioavailability, which is the key factor reflecting the potential
influence of microplastics on different species, depends on both the
properties of the pollutant and the foraging preferences of the or-
ganisms (Setala et al., 2016). Unlike most selective forgers, organ-
isms exhibiting generalist feeding preferences and prey capture
methods (e.g., predators only distinguish food from other sub-
stances based on limited characteristics) are more likely to ingest
microplastics with similar features to their natural prey (Peters
et al., 2017). Physical properties affect the morphology and
mobility of microplastics within the aquatic environment, which
affects bioavailability by altering the distribution within the aquatic
environment, presenting a similar appearance to natural sub-
stances and causing different extents of physical damage to the
organism. The most studied physical properties include the size,
color, density and shape of microplastics, and each of the properties
contributes differently to the negative effects.
2.1.1. Size
Microplastics occupy the same size range as sand grains,
microalgae and plankton, which are available to a wide range of
aquatic organisms, especially the nonselective foragers (Baldwin,
1995). The microplastic uptake rate by Daphnia magna has shown
an exponential correlation with size, and the number of daphnids
with microplastics in their guts decreases with the increase in the
average particle size (Kokalj et al., 2018a). The most frequent size of
microplastic ingested by daphnids was below 100 mm, which is
consistent with the food size preference of daphnids (Kokalj et al.,
2018a). Compared to daphnids, Artemia franciscana ingested fewer
microplastic particles under the same microplastic exposure con-
ditions due to its smaller food feeding preferences (<50 mm)
(Ferna
ndez, 2001). For the amberstripe scad Decapterus muroadsi
(Carangidae) fish, the most commonly ingested microplastics are
similar in size to their prey, at approximately 1.3 ± 0.1 mm (Ory
et al., 2017). After ingestion, the particle size is also a crucial fac-
tor determining the translocation ability of microplastics within the
body of an organism. The smaller microplastics (~3.0 mm) trans-
locate within Mytilus edulis more easily and readily than the larger
particles (~9.6 mm) (Browne et al., 2008). The translocation of
microplastics from the digestive tracts to other tissues within the
brown shrimp Crangon crangon (L.) was negligible when the par-
ticle size was larger than 20 mm (Devriese et al., 2015). Thus, for this
specific species, the smaller microplastics showed higher
bioavailability due to the higher ingestion rate and the trans-
location rate within the organism. On the other hand, for different
species, the biological responses also varied with the diverse food
size preferences and the body size of the organisms. For instance,
the 0.05 mm microplastics caused the highest toxicity for the
monogonont rotifer Brachionus koreanus because smaller micro-
plastics have higher retention times and thus can exert negative
effects due to low egestion efficiency (Jeong et al., 2016). For Cae-
norhabditis elegans, the 1.0 mm particles caused the highest
lethality, maximum accumulation, lowest Ca2þ level in the intestine
and highest expression of glutathione S-transferase 4 compared to
both the larger (0.1 mm) or smaller (5.0 mm) microplastics, since the
1 mm microplastic induced severe intestinal damage (Lei et al.,
2018). The general pattern for differing impacts of different
microplastics sizes for different species remains unclear, yet the
 H. Ma et al. / Environmental Pollution 261 (2020) 114089
bioavailability of microplastics is affected by the diverse morphol-
ogies and physiological structures of organisms, which are directly
related to the ingestion likelihood, egestion rate and translocation
potential. Therefore, precise representitive model organism should
be selected for toxicological studies based on the aims and targets
of the research. It is also noteworthy that the controlled micro-
plastics of uniform size that are used in research do not align with
the sizes in the actual aquatic environment. The voluntary food
intake behavior of organisms should be considered by exposing
organisms to a wider ranges of microplastic sizes. The compre-
hensive consideration of both the range of microplastic sizes in the
aquatic environment and the features of the native species is crit-
ical for obtaining reliable results during ecotoxicological tests or
risk assessments.
2.1.2. Color
Color is another aspect of microplastics that disturbs foraging by
visual predators with various ingestion biases. For instance, 80% of
the amberstripe scads (Decapterus muroadsi) in a previous study
ingested mainly blue polyethylene fragments, which presented a
similar morphology in color and size with their blue copepod prey
(Fig. 1) (Ory et al., 2017). Mostly dark colors of microplastics,
especially green microplastic fibers, which resembled marine
plankton, were found in the digestive systems of flathead grey
mullet Mugil cephalus (Cheung et al., 2018a). The white, clear and
blue microplastics, which are similar in color to the plankton in the
area, were the most common colors of the microplastics ingested
by the planktivorous fishes in the North Pacific central gyre due to
the resemblance to the food source of the fishes (Boerger et al.,
2010). Thus, the ingestion propensity of visual predators for
microplastic is significantly affected by the color. In addition to its
impact on the ingestion preferences, the color was also studied as
an intuitive indicator reflecting the potential toxicity of micro-
plastics. The enrichment of PAH in microplastics composed of
polyethylene and polypropylene showed no difference, while a
predictable increase in the PAH concentration was observed along
with the darkening of the color (Fisner et al., 2017). Moreover, the
lighter colored microplastics are prone to having lower molecular
weight PAH, and darker microplastics contain higher weight PAH
(Fisner et al., 2017). This adsorption capacity variation with color
Fig. 1. The microplastics resembling the prey were more likely to be ingested (blue microplastic debris ingested due to the confusion with the blue copepods (Ory et al., 2017))
(Obtained copyright permission, Science of the Total Environment, Elsevier, 4543940873342, Mar 07, 2019). (For interpretation of the references to color in this figure legend, the
reader is referred to the Web version of this article.)
3
difference also revealed that the black microplastics tended to
adsorb more chemicals, such as PCBs and PAHs, than the white ones
(Antunes et al., 2013). As a result, the organisms would bear addi-
tional stress from the enriched contaminants throughout the cir-
culatory system, tissues and organs due to ingestion along with
microplastics. One possible reason could be that pigments with
different color are beneficial to the adsorption capacity of micro-
plastics (Frias et al., 2013). Additionally, the color could reflect the
relative age and degree of weathering of the microplastic. The af-
finity between the microplastic surfaces and contaminants is
affected, and the loss of the pollutants on the surface of the
microplastic during weathering results in a low degree of adsorp-
tion. The direct relationship between color and pollutant enrich-
ment is a new finding in toxicological research. The underlying
mechanisms from the aspects of the chemical composition and
how the microplastics with different colors behaved in the aquatic
environment should be studied further. Moreover, considering the
ingestion preference of the organisms and the predictable variation
of the contaminant enrichment, monitoring of the microplastic
color spectrum could be beneficial to the preliminary assessment of
microplastic toxicity for organisms with different feeding
preferences.
2.1.3. Density
Density influences the distribution and destination of micro-
plastics by affecting the trajectory, sinking velocity and spatial
distribution of microplastics, which further affects the microplastic
distribution in the different biota and habitats. For instance, the
spread of low-density plastics over the surface water impedes the
photosynthesis of the algae and the respiration of the zooplankton
(Song et al., 2014), high-density microplastics have been consis-
tently detected in the digestive tracts of the benthic invertebrates
(Naidu et al., 2018; Nakki et al., 2017), and the microplastics that
sink to the sediments on the seafloor endanger the deep ocean
biota (Courtene-Jones et al., 2017a).
Moreover, the low-density microplastics ingested by copepods
from the surface water are excreted in a mixture with the feces after
digestion. The density change alters the sinking velocity of the
copepod-egested fecal pellets, which are important food sources
for fish, polychaetes, crustaceans and copepods. Consequently, the
4 H. Ma et al. / Environmental Pollution 261 (2020) 114089
food distribution for marine organisms may be impacted, and the
bioavailability of microplastics is aggravated during feeding (Cole
et al., 2016). Furthermore, contaminants such as polycyclic aro-
matic hydrocarbons (Fries and Zarfl, 2012), polychlorinated bi-
phenyls (Mato et al., 2001), and phenanthrene (Karapanagioti and
Klontza, 2008) tend to have higher diffusion coefficients in low-
density microplastics than in high-density microplastics, which
directly affects microplastic toxicity. Therefore, the density of
microplastics in further toxicological studies should be considered
as a property with the potential for 1) altering the exposure
pathway of the contaminants along with the microplastics, 2)
inducing combined toxicity effects with other pollutants, and 3)
causing ecological turbulence by disturbing the distribution of food
in the aquatic environment.
2.1.4. Shape
The shape of microplastics is a critical morphological feature
that has been generally divided into regular and irregular shapes,
affected by the initial shape, the aging and weathering conditions.
More specifically, microplastics can also be classified as spheres,
fibers, fragments, pellets, films, and flakes (Albanese et al., 2012).
The shape alters the hydrodynamic characteristics of microplastics,
which relates to a series of biological and toxicological effects by
disturbing the distribution and bioavailability. Unlike density,
shape affects the dynamics of microplastics indirectly. The settling
velocity of microplastics in aquatic environments varies due to their
varying shapes (Khatmullina and Isachenko, 2017). Plastic fibers
and thin films show higher buoyancy and lower settling velocity
than spherical plastic particles even the debris have the same
density and volume (Filella, 2015; Zhang, 2017). Based on simplified
physical models and geometrical considerations, the transport
times of polystyrene microplastics in the aquatic environment
follow the order of foamed polystyrene<polystyrene fibres<-
spherical polystyrene particles (Chubarenko et al., 2016). Since the
predation processes of most aquatic organism are also dynamic, the
changes in the microplastic settling and eventual fates due to
different morphological shapes indirectly affect the opportunities
for ingestion and the bioavailability.
After ingestion, the shape of the microplastics also affects the
egestion and residence time within the body. For example,
D. magna rapidly ingests both regularly and irregularly shaped
polyethylene microplastic particles, but the gut clearance and
apparent gut residence times of the irregular microplastic particles
were longer than those for the regular shaped microplastic parti-
cles, which were even accompanied with more pronounced acute
inhibitory effects (Bayo et al., 2017). The microplastic fibers inges-
ted by the amphipod Hyalella azteca required longer clearance
times than the spheres, and higher toxicities were found for the
microplastic fibers, which were attributed to longer residence
times because of the shape (Au et al., 2015). Discharged plastic
debris with the same composition behaves differently in the
aquatic environment, and the threats caused by irregularly shaped
microplastics tend to be higher due to the difficulty of egestion and
clearance for organisms compared to the regular spherical
particles.
2.2. Chemical properties
The chemical nature of microplastics is determined by the
plastic composition and synthesis methods and is expressed as
various chemical characteristics, such as different functional
groups, surface polarities, stabilities, and crystallinities, which
enable the identification of the microplastics with the potential to
leach additives from particles or to accumulate environmental
pollutants on the surface. Unlike the physical properties that
directly affecting ingestion, egestion or cause physical injury to
organisms, the chemical properties of microplastics are related to
their persistence affinity for chemicals. The patterns of enrichment
with contaminants and the release of additives change with the
prevalence of microplastics; thus, the changes in the behavior of
the microplastics are discussed from the aspect of the chemical
properties.
2.2.1. Functional groups & affinities with pollutants
The functional groups and polarities of microplastics contribute
the most to the accumulation of contaminants from the ambient
environment (Fig. 2). The partition coefficient Kd of per-
fluorooctanesulfonamide (FOSA) with different microplastics fol-
lows the order of polyethylene (Kd(PE) ¼ 298.3 L/kg)>polyvinyl
chloride (Kd(PVC) ¼ 115.7 L/kg)>polystyrene (Kd(PS) ¼ 84.9 L/kg). The
highest Kd for the nonpolar PE has been attributed to the strong
hydrophobic affinity between the microplastic and the symmetric
nonionic FOSA. The benzene rings on PS cause steric hindrance of
the bond rotation and decrease the free volume between the
chains, leading to the low sorption levels (Wang et al., 2015). The
adsorption of the antibiotics sulfadiazine (SDZ), amoxicillin (AMX),
tetracycline (TC), ciprofloxacin (CIP) and trimethoprim (TMP) on
the 5 types of microplastic polyethylene (PE), polystyrene (PS),
polypropylene (PP), polyamide (PA), and polyvinyl chloride (PVC)
depends on the hydrogen bonding, hydrophobic interaction, van
der Waals forces and electrostatic interactions, and the highest
adsorption capacity of PA with antibiotics is attributed to the strong
H-bonding with the amide groups (Li et al., 2018). The adsorption
behavior of polyethylene (PE), polystyrene (PS) and polystyrene
carboxylate (PSeCOOH) with 18 perfluoroalkyl substances (PFASs)
follows the order PS>PS-COOH>PE, and the influence of the hy-
drophobic interaction between PFASs with microplastics has been
shown to increase the toxicity of hydrophobic contaminants to
organisms and aquatic ecosystem (Llorca et al., 2018). In addition to
pollutant accumulation, the functional groups on microplastics
may also directly interfere with microplastic toxicity. For instance,
no significant difference between the adsorption of Ni on PS and
PS-COOH was found, yet the toxicity of Ni mixed with PS-COOH was
higher than that with PS. The detailed mechanism for this phe-
nomenon remains unclear; nevertheless, the combined effect
suggests that the toxicity of pollutants varies with the different
functional groups of microplastics (Kim et al., 2017).
2.2.2. Crystallinity
In aquatic environments, the crystallinity of an adsorbent may
affect the separation of the HOC (hydrophobic organic contami-
nants) from carbohydrates and other semicrystalline (biological)
polymers (Hung et al., 2010). Organic adsorbents in the environ-
ment are composed of organic polymers that contain both crys-
talline and amorphous phases. The crystalline areas are categorized
by molecules or molecular segments that are usually arranged in
lattices. In contrast, the amorphous regions have randomly ar-
ranged molecules, thus showing a loose and flexible structure that
is more similar to that of a liquid. The adsorption of HOC usually
occurs on the amorphous areas due to its internal structure, which
is characterized as glassy or rubbery. The adsorbent could be
considered a mixture of glass and rubber polymers. Organic pol-
lutants tend to have higher affinities for rubber plastics than for
glass plastics (Wu et al., 2001; Guo et al., 2012; Rochman et al.,
2013). The polymer portion of the glass phase has higher adhe-
sion and more concentrated force, while the polymer segment of
the rubber phase shows greater fluidity and flexibility and can be
considered as a dynamic viscous liquid. Because of their rigidity,
glass polymers have a long life and closed internal nanoholes,
which can act as adsorption sites for organic contaminants in water.
 H. Ma et al. / Environmental Pollution 261 (2020) 114089
Fig. 2. The molecular structures of the most common microplastics and the interactions with environmental contaminants.
The characterization of crystallinity could facilitate further assess-
ments of the affinity between microplastics and environmental
pollutants.
2.2.3. Stability
The additives used during plastic synthesis, such as monomers,
oligomers, pigments, reinforcements, and plasticizers, usually
present high toxicity to organisms. The weathering alters the
properties of microplastics and accelerates the release of some
superfluous compounds from the microplastics (Liu et al., 2019),
threatening the ecological health of aquatic ecosystems. Significant
enrichment of hexabromocyclododecanes (HBCDDs) has been
found in marine sediments and mussels, and the subsequent
research to identify the source confirmed that HBCDDs were
leached from expanded polystyrene (EPS), which is a widely used
material in aquaculture farming. In addition, the acute toxicity of
leachates from different plastics varies differently after irradiation
and weathering. To test the toxicity caused by the low stability,
twenty-one types of plastic debris were irradiated with artificial
sunlight; 38% of these microplastics had leachates that resulted in
acute toxicity to the marine harpacticoid copepod Nitocra spinipes
(Bejgarn et al., 2015). Both the plastic-derived chemicals bisphenol
A (BPA) and di-2-ethylhexyl phthalate (DEHP) have been reported
to cause 1.2- to 50-fold reductions in biomass and to perturb the
photosystem and photosynthetic activity of the marine toxic
dinoflagellate Alexandrium pacificum (M’Rabet et al., 2018). Expo-
sure experiments with microplastics made from polyethylene
terephthalate (PET) and its associated plasticizer Di(2-ethylhexyl)
phthalate (DEHP) with the calanoid copepod Parvocalanus crassir-
ostris showed that the nauplii were severely impacted even at low
chemical concentrations, presenting a 48 h LC50 value of 1.04 ng/L.
DEHP did not show a significant impact on the adult copepods.
However, the egg production of the copepods was reduced under
the sublethal concentration of DEHP or the microplastic (Heindler
et al., 2017). This induction of a heritable reproductive disorder
by the microplastic and its plasticizer poses a potential threat to
subsequent generations of copepods and even the organisms at
higher trophic levels. In addition, not only the organic additives but
also the release of the total organic carbon, Cl, Ca, Cu, and Zn from
the aged microplastics were significantly increased due to photo-
oxidation in the aquatic environment. New adsorption bands of
eC]O eCeO and eOH were formed during the aging process,
which emphasizes the importance of analyzing the stability of
microplastics during toxicity tracking research and risk assess-
ments (Bandow et al., 2017).
2.2.4. Surface charge
The surface charge of microplastic has rarely been discussed in
comparison with the functional groups and the polarity; however,
the contribution to microplastic toxicity is nonnegligible. The
5
embryotoxicity test of PS-COOH and PS-NH2 for embryos of the sea
urchin Paracentrotus lividus suggested that the status of the charges
(i.e., þ/) caused various dispersion patterns of the microplastics
inside the bodies of the studied organisms, and only PS-NH2 dis-
rupted the cell membrane and caused oxidative stress, which
eventually induced cell death by apoptosis in the sea urchin em-
bryos (Vega and Epel, 2004). The opposite surface charges of
microplastics and natural organic matter compounds and minerals
also facilitate their interactions in aquatic environments. The
nanoscale materials in natural media are generally charged, and the
heteroaggregation with microplastics due to opposite surface
charges further influences the uptake rate by biota and the bio-
distribution of this nutrient matter, disrupting the essential phys-
iological functions linked to the feeding and growth of organisms
(Oriekhova and Stoll, 2018; Qiao et al., 2019a). Both the neutral and
positively charged microplastics increased TiO2 NP toxicity for the
marine algae Chlorella sp., and the oxidative stress followed the
trend TiO2 NPs þ Plain PS/ NH2-PS > TiO2 NPs þ COOH-PS
(Thiagarajan et al., 2019).
3. Spatiotemporal dynamics (distribution) affect microplastic
ingestion by organisms
While the pressure of microplastics on aquatic ecosystems is
increasingly recognized, the understanding of the spatiotemporal
dynamics of microplastics remains limited. The spatial dynamics
reflect the distribution and pollution conditions of microplastics,
and the temporal dynamics provide information on the fluctuations
of microplastic contamination over time. The lack of comprehen-
sive consideration of the distribution dynamics may lead to biases
in contamination monitoring and risk assessments. Therefore, the
features of the spatiotemporal distribution provide a better un-
derstanding of the occurrence of microplastics within aquatic
ecosystems as well as the dynamic toxicity patterns.
3.1. Spatial distribution
The microplastics in aquatic environments travel around the
world, driven by the orientation of the coastline and the local wind
and wave conditions (Allen et al., 2019; Rezaei, 2019). An annual
microplastic survey of three exposed beaches on the Canary Islands
confirmed the migration of portable microplastic debris of nonlocal
origin from the North Atlantic Ocean, driven by the southward-
flowing Canary Current (Herrera et al., 2018). The lateral
geographical distribution of microplastics in the global ocean far
from the polar region was reviewed, and the modeling approaches
for predicting the fate and prevalence of microplastics were sum-
marized (Lusher, 2015; Law et al., 2014). Therefore, in this study, the
vertical spatial distribution of microplastics in aquatic environ-
ments and the ecological impact were discussed in depth.
6 H. Ma et al. / Environmental Pollution 261 (2020) 114089
According to the distance travelled by sunlight, the ocean is
vertically divided into the euphotic zone (0e200 m), disphotic zone
(200e1000 m), and aphotic zone (deeper than 1000 m) (Hedgpeth,
1957). The phytoplankton, zooplankton, forage fish and predator
fish are the most affected by the widespread light-weight micro-
plastic in the euphotic zone and have been most frequently re-
ported in recent decades. Moreover, the accumulation of
microplastic particles also occurs within the sea surface microlayer,
which is the naturally reactive boundary layer between the water
and atmosphere (Song et al., 2014). The accumulated microplastics
within the microlayer affect the photochemical reactions by inter-
fering the sunlight irradiation in this region. As a result, the
photosynthesis, respiration and physiological activities of the
plankton are further impacted. With the presence of microplastics,
the growth of the algae Skeletonema costatum was inhibited (Zhang
et al., 2017), and the roots of a floating plant, the duckweed Lemna
minor, were mechanically blocked (Kalcikova et al., 2017). In addi-
tion, the potential risk of microplastics acting as a substrate for
reactions between complex compounds, such as inorganic com-
ponents, dissolved organic matter, or contaminants enriched in the
surface microlayer, is another severe issue that may trigger diverse
photochemical reactions within the euphotic zone.
The prevalence of microplastics below the euphotic zone mainly
depends on the diel vertical migration (DVM) of the active meso-
pelagic fishes that transfer microplastics from the sea surface to the
disphotic zone and the aphotic zone. The mesopelagic fishes show a
high ingestion rate for microplastics regardless of the species,
location, or migration behavior, and the movement of mesopelagic
fish from the euphotic zone to the deep sea mediates the transfer of
microplastics to unexposed species and regions of the ocean
(Lusher et al., 2016; Davison and Asch, 2011). This phenomenon was
further confirmed by in situ feeding experiments with the large
larvaceans Bathochordaeus, which indicated that the microplastics
from the sea surface could be delivered to the seafloor via biological
interference (Katija et al., 2017). The ecological consequences are
still poorly understood, but the unpredictable movement of the
mesopelagic fish has facilitated the abundant occurrence of
microplastics throughout a wide area of the oceans, and the further
impact on the aquatic ecosystem remains unknown. For the aphotic
zone of the ocean, microplastics are found ubiquitously on the
seafloors of the Southern Ocean, North Atlantic Ocean, Gulf of
Guinea, and the Mediterranean Sea (Van Cauwenberghe et al.,
2013). The microplastics were moved through the ocean and sunk
into the deep sediment, invading one of the most pristine and
vulnerable areas of the marine environment. The ingestion of
microplastics by lysianassoid amphipods at the deepest location of
all the Earth’s oceans was detected (Jamieson et al., 2019). The
occurrence at the seafloor suggests a long-term exposure of benthic
ecosystems to microplastics (La Daana et al., 2019).
3.2. Temporal dynamics
Seasonal climate change influences the temporal variation in
disturbance from microplastics. The significant differences in the
microplastic amounts sampled from Lambra (La Graciosa Island)
and Famara (Lanzarote Island) presented seasonal occurrence pat-
terns of microplastics in aquatic environments, which is attributed
to the local-scale wind and the seasonal wave condition variation
(Herrera et al., 2018). In the Pearl River in China, the density of
plastic debris in the rainy season was reported to be significantly
higher than that in the dry season because of the larger amount of
river discharge (Cheung et al., 2018b). The weak management of
plastic pollution in inland environments allows flooding in urban
areas to flush the discharged plastic debris into the ocean. A com-
parison of the microplastic occurrence from December 2016 to
January 2017 in Mersin Bay suggested that the seasonally heavy
rains and floods increased the microplastic abundance in the
aquatic environment over time; after being flushed by the floods,
the average microplastic size decreased from 2.37 mm (preflood
period) to 1.13 mm (postflood period) (Gundogdu et al., 2018). As a
consequence of this seasonal occurrence pattern, the seasonality of
organism assemblages could be threatened by changes in the
microplastic bioavailability over time.
The distribution of microplastics, zooplankton and the fish
larvae in the mangrove creeks of the Goiana Estuary, Brazil, changes
with the lunar cycle due to the different tidal current regimes. The
higher abundance of microplastic threads was revealed, while there
were fewer zooplankton available in the creeks (Lima et al., 2016).
Such dynamic variation in both the aquatic species and the
microplastic occurrence leads to seasonal differences and diverse
threats to different species. For example, more microplastics were
detected during summer than spring in the digestive tracts of two
economically and ecologically crucial planktivorous forage fish, the
Atlantic herring (Clupea harengus) and the European sprat (Sprattus
sprattus), in the Baltic Sea. The variation in uptake was mainly due
to the seasonal difference in feeding activity, which reflected the
variation in the vulnerability of the organisms at different devel-
opmental stages (Beer et al., 2018). It is also interesting that zoo-
planktivores were likely to feed on more microplastics than natural
prey before the rainy season. Before the rainy season, the mer-
oplankton in the macrobenthos could be confused with paint par-
ticles, whereas styrofoam could be mistaken for immature
copepods by predators (Kang et al., 2015). The possible explanation
for this phenomenon could be the lower microplastics abundance
after the rainy season or the behavioral plasticity for the nonspe-
cific food selection ability of the predator.
The interference of the temporal dynamic of the microplastics
tends to be complicated and versatile, and the physicochemical
parameters and nutritional quality of the habitat directly influence
the living conditions of the organisms (Hashemi et al., 2019). A
better understanding of seasonal fluctuations and the subsequent
influence induced by the microplastics comes from the accuracy
and importance of the research. To achieve a comprehensive un-
derstanding of the ecological disturbance caused by microplastics,
both the spatial and temporal dynamic patterns of microplastics
should be considered in relation to the seasonal activity of organ-
isms during pollution monitoring, toxicological tests, and the sub-
sequent analysis of the instability of ecological health.
4. How do organisms respond to the microplastic toxicity?
Many studies have investigated the microplastic-induced
adverse effects on organisms, which range from disruption of
physiological functions to lethal effects. Based on the fate of
microplastics after ingestion, microplastic toxicity could be classi-
fied as follows:
1) accumulation within the digestive tract, causing physical dam-
age such as clogging and injury;
2) discharge as pseudofeces, which disturbs the energy flow of
organisms;
3) translocation within the body, which exposes the internal tis-
sues and organs to microplastics.
The overall generalization of the microplastic-caused adverse
effects on organisms was summarized to establish a sound research
framework for future microplastic toxicological studies and to
assess the potential ecological disturbances on a large scale.
 H. Ma et al. / Environmental Pollution 261 (2020) 114089
4.1. Physical damage
Physical damage is the most apparent effect from the ingestion
of microplastics by organisms. The most common damages include
intestinal blockage, cracking of villi and splitting of enterocytes (Lei
et al., 2018). Furthermore, tissue alteration also occurred even after
the ephemeral occurrence and accumulation. Structural changes in
the gills and digestive glands, as well as necrosis in other tissues,
such as the mantle have been observed in mussels after micro-
plastic ingestion (Brate et al., 2018; Faggio et al., 2018). The more
detailed and specific physical impacts of microplastics were
reviewed by Wright et al. (2013a). In the present review, the subtle
yet profound interference with energy storage, metabolism, phys-
iological behavior and survival of organisms is further addressed
below.
4.2. Energy budget disturbance
Organisms generate false satiation after the ingestion of
microplastics, which consequently disrupts their regular nutrition
and energy intake and leads to abnormal physiological responses.
Studies of the disturbance of the energy budget caused by micro-
plastics have been conducted by monitoring the influence on
ingestion, respiration, growth and excretion of organisms. The
filtering activity of the blue mussel (Mytilus edulis) was reduced
after the ingestion of 100 nm polystyrene microplastics, and the
feeding activity was further affected (Wegner et al., 2012). The
weight of the polychaete worm Arenicola marina was changed by
suppressed feeding activity due to microplastics, which reflected an
up to 50% depletion of the energy reserves (Wright et al., 2013b).
The ingestion of foods containing microfibers (0.3e1 wt%) by the
crab Carcinus maenas also reduced the food consumption from 0.33
to 0.03 g/d, and the energy available for growth for the crab
decreased from 0.59 to 0.31 kJ crab/d (Watts et al., 2015). The
disturbance of the energy budgets of the organisms was always
accompanied by the production of pseudofeces, and the growth
and performance were obstructed as a consequence of the reduc-
tion in energy intake and depletion of energy reserve depletion.
According to the Wilby 1988 scoring system, the morphology of
Hydra attenuate also changed significantly after the ingestion of
microplastics (Murphy and Quinn, 2018). The body length of Cae-
norhabditis elegans was significantly reduced after 2 days of
microplastic exposure due to the decreased energy assimilation (Lei
et al., 2018). The development of Paracentrotus lividus plutei with
different body lengths and arm lengths indicated the interference
of microplastics during postembryonic development; in Ciona
robusta, metamorphosis was inhibited at an early life stage
(Messinetti et al., 2018).
Different species can only function well in an ecosystem when
the individual organisms maintain healthy physiological states. The
ingested and accumulated microplastics are transferred to higher
trophic levels, and such energy deficiency in individual organisms
impedes the energy uptake, development and population of the
species and subsequently disturbs the energy flow through the
entire food web (Xu et al., 2017).
4.3. Translocation within the body of an organism
After ingestion, subsequent microplastic trafficking was
observed in different organs of organisms, which was followed by
gradual yet incomplete renal clearance (Fig. 3). Cytotoxicity
research on different nanoparticles suggests that the nature of
endocytosis and particle-cell interactions provides particles with a
pathway to expose tissue and organs (Livadaru and Kovalenko,
2006; Roiter et al., 2008). After crossing biological barriers (such
7
as cell membranes), the microplastics translocated from the
digestive system through both active and passive physical pene-
tration have a considerable impact on biological processes, even
causing long-lasting and irreversible damage to organisms
(Vakarelski et al., 2007; Leroueil et al., 2008; Forouhar Vajargah
et al., 2019; Forouhar Vajargah et al., 2018). Although the crucial
factors for the penetration capability of microplastics remain poorly
understood, the translocation of microplastics within the body has
been shown to induce complicated sublethal responses to organ-
isms (Table 1).
4.4. Metabolism and sublethal responses
The internal exposure of microplastic to the circulatory system,
tissue and organs results in metabolic disorders and sublethal re-
sponses in organisms, which reflected in endocrine disorders,
oxidative stress, immune responses, and altered gene expression
(Qiao et al., 2019b). The metabolism and growth of an organism are
simultaneously critically affected by microplastic ingestion. The
polystyrene microplastics in the guts of the adult zebrafish
increased the volume of mucus and triggered inflammation after
ingestion. The high-throughput sequencing of the 16S rRNA gene
V3eV4 region and the operational taxonomic unit analysis revealed
an in-depth response at the phylum and genus levels, suggesting
that the microplastic exposure within the gut changed the richness
and diversity of the microbiota, leading to a microbial imbalance
(Jin et al., 2018). The oxygen consumption of the shore crab Carcinus
maenas showed a dosage effect from microplastic exposure; sub-
sequently, a small but significant decrease in the hemolymph so-
dium ions and an increase in the calcium ions were observed
(Watts et al., 2016). Another example is that the reactive oxygen
species (ROS) produced during the phagocytosis of the nano-
particles could act as an indicator for cytotoxicity (Burgos-Aceves
et al., 2018). A significant size-dependent increase in the ROS
levels in the monogonont rotifer Brachionus koreanus was observed
with microplastic exposure. The activation of antioxidant-related
enzymes as defense mechanisms further proved the oxidative
stress induced by the microplastic (Jeong et al., 2016).
In further reports, the endocrine system function of the Japa-
nese medaka Oryzias latipes was disturbed under microplastic
exposure at environmentally relevant concentrations, and gene
expression was observed to be altered after chronic two-month
dietary exposure. It is quite relevant that the dosage severely in-
fluences and regulates choriogenin (Chg H) gene expression in
males as well as vitellogenin (Vtg I), choriogenin (Chg H) and es-
trogen receptor (ERa) gene expression in females. The histological
observation also shows the abnormal proliferation of germ cells in
one male fish (Rochman et al., 2014).
Moreover, a transcriptome analysis showed that the micro-
plastic particles were integrated into the immunological recogni-
tion process of the zebrafish larvae and that the nuclear receptors in
the lipid metabolism and toxicity pathway were enriched, and the
colocalization of neutrophils and macrophages was found around
the PS particles (Veneman et al., 2017). In another report, a signif-
icant neurotoxic effect and oxidative stress was observed in the
Amphibalanus amphitrite barnacle and Artemia franciscana brine
shrimp triggered by microplastic accumulation. The low enzymatic
activity from the damage and the presence of the defense bio-
markers cholinesterase (indicative of neurotoxicity) and catalase
(indicative of oxidative stress) suggested that the microplastics
disturbed the detoxification of hydrogen peroxide in the organisms
(Gambardella et al., 2017). Underlying the phenomenal inhibitory
effect of microplastics on the body length, reproduction and sur-
vival rates of the nematode Caenorhabditis elegans, the increased
expression of the glutathione S-transferase 4 enzyme in the
8 H. Ma et al. / Environmental Pollution 261 (2020) 114089

Fig. 3. a. The microplastics translocated within the zebrafish larvae away from the injection site (Veneman et al., 2017) (obtained copyright permission, Aquatic Toxicology, Elsevier,
4543950272607, Mar 07, 2019); b. accumulation of polystyrene microbeads in the gills, liver, and gut of Eriocheir sinensis (Yu et al., 2018b) (obtained copyright permission, Aquatic
Toxicology, Elsevier, 4543950630725, Mar 07, 2019).

Table 1
The translocation of microplastic within different species (a. Biological response reported in the research; b. Potential impact proposed in the literature).

Species Translocation spot Biological response & Potential impact Ref.

b
Bivalve mussel Circulatory system, Restricting blood flow causing damage to the vascular tissues and changes in cardiac activity Browne et al.
Mytilus edulis hemolymph (2008)
(L.)
b
Invertebrate Lipid storage droplets Decreasing energy reserves for metabolism and growth; Transfer from mother to newly created egg Rosenkranz
Daphnia Magna et al. (2010)
Fiddler crab Gills, stomach, hepatopancreas Reducing ecosystem service (e.g., processing of organic matter) due to the low performance of Brennecke
Uca rapas organisms, leading to far-reaching consequences for the coastal habitats b et al. (2015)
Mussel Mytilus Hemolymph, tissues Bioaccumulation and biomagnification during the trophic transfer between mussel and crab, leading to Farrell and
a
edulis (L.) Stomach, gills, and ovary vulnerable larval and juvenile stages of the crab Nelson (2013)
Shore crab
Carcinus
maenas
b
Gilt-head Liver, muscles Causing inflammation, lipid accumulation, oxidative stress at higher exposure concentration Jovanovic et al.
seabream (2018)
Sparus aurata
Zebrafish larvae The heart region Triggering systemic immune responses Veneman et al.
(2017)
European Hepatic Tissue Leaching chemicals (adsorbed pollutants and additives) into the blood and other organs; enhanced Collard et al.
anchovies vascular thrombosis b (2017)
Engraulis
encrasicolus, L
Barnacle larvae Bloodstreams to tissue and Included in metamorphosis and settled into the juvenile form, persisting in other parts of the body and Bhargava et al.
Amphibalanus other parts of the body tissues throughout stages of growth and development a (2018).
amphitrite
Blue Mussel Adopted into cells of the Causing significant effects on the tissue and cellular levels, histological changes, and inflammatory von Moos et al.
Mytilus edulis L., digestive system response a (2012).

intestine suggests that intestinal damage and oxidative stress may 4.5. The impact on behavioral pattern, fecundity, and survival
be the major mechanisms for the toxic effects of microplastics (Lei
et al., 2018; Alomar et al., 2017). The disruption of behavioral patterns, fecundity and survival are
 H. Ma et al. / Environmental Pollution 261 (2020) 114089
regarded as the ultimate toxicological responses of organisms un-
der stress from anthropogenic alterations to the environment
(Wong and Candolin, 2015). The chronic exposure of Ceriodaphnia
dubia to microplastic fibers had a dose-dependent effect on energy
loss and physical damage, leading to reduced growth and repro-
duction (Ziajahromi et al., 2017). In a similar investigation of the
toxicity and impacts of microplastic, it was observed that the
mortality of the Asian green mussel Perna viridis was increased due
to energy reserve depletion, which affected the essential life
functions (Rist et al., 2016).
Moreover, the abnormal behaviors reflect the distempered
physiological functions of the organisms, which impact individual
development and life survival under harsh environmental condi-
tions. The jump height of the beachhopper Platorchestia smithi was
reduced after ingesting microplastic particles (Tosetto et al., 2016).
The swimming activity of marine crustaceans was altered under
microplastic exposure, and the swimming speeds of Amphibalanus
amphitrite and Artemia franciscana were inhibited significantly due
to the mechanical disturbance caused by microplastic agglomera-
tion (Gambardella et al., 2017). Similarly abnormal swimming ac-
tivity was also observed; the water flea C. dubia becomes entangled
in microplastic clusters, which results in an inability to swim
(Ziajahromi et al., 2017). The changes to physiological activity could
further interfere with their feeding activity and ability to avoid
predators.
Notably, the changes to the behavioral patterns also reflect the
subhealthy status, potential fecundity interference and the
increased mortality of organisms, which are warns for subsequent
ecological effects from the superficial phenomenon. For instance,
further investigation of the reduction in the jump height of the
beachhopper Platorchestia smithi revealed that the beachhoppers
also suffered from microplastic translocation from the gut to the
gills. The survival rate was reduced simultaneously with the
behavioral alternation. Thus, the abnormal behavioral patterns of
species could act as an indicator of the microplastic burden on the
vital activities of organisms (Tosetto et al., 2016).
4.6. Combined effects of the inorganic and organic pollutants
Beyond the direct toxicity caused by microplastics that was
discussed above, the combined effects of the microplastics and
environmental contaminants cause worsened contamination. The
enduring plastic debris drifting in the aquatic environment acts as a
reservoir or vector, accumulating widespread trace pollutants,
leading to long-distance transport and high bioavailability of hy-
drophobic and toxic contaminants for organisms. The desorption of
chemicals under the conditions in the gut is reported to be 30 times
higher than that in seawater (Bakir et al., 2014), and the toxicity of
both the microplastic and environmental pollutants tends to be
more detrimental due to the combined effects (Table 2). Consid-
ering the potential for bioaccumulation and biomagnification
within aquatic ecosystems, the combined toxicity effects of
microplastics with different contaminants have been widely stud-
ied in recent decades.
5. What ecological consequences will be triggered by the
disturbances from microplastics?
How is the ubiquity of microplastics related to the function of
aquatic ecosystems? To maintain an intact aquatic environment,
different environmental elements and all species provide valuable
ecological services for the ecosystem. However, by altering natural
habitats; disturbing the bacterial community; disrupting the
development of species, populations and communities develop-
ment; and indiscriminately interfering with the indispensable
9
ecological functions of the ecosystem, widespread microplastics
jeopardize basically every process in an ecosystem. These distur-
bances are known to threaten ecosystem stability, but forecasting
the direct outcomes from scattered evidence is not yet possible. For
an improved understanding of the linkage between environmental
perturbations and the prevalence of microplastics, identifying the
distress signals that foretell major disruptions to ecology may one
day predict, or perhaps even prevent, the potential destabilization
of ecosystems.
5.1. Ecosystem productivity disturbance
The prosperity of aquatic ecosystems is supported by steady
ecosystem productivity, and primary production plays a funda-
mental role in structuring aquatic food webs. However, the ubiquity
of microplastics as a human-driven environmental change may
lead to losses in ecosystem productivity by obstructing nutrient
production and cycling within ecosystems. By using salps as model
organisms under environmentally relevant concentrations, micro-
plastics were detected in the fecal pellets. Under potential future
scenarios, up to 46% of fecal pellets are predicted to contain
microplastics, which would lower the efficiency of biological
pumps in driving sequestration of the anthropogenic carbon in the
ocean (Wieczorek et al., 2019). Moreover, the interactions between
the microalgae Skeletonema costatum and microplastics, such as
adsorption and aggregation, reduce the algal chlorophyll content,
resulting in low photosynthetic efficiency. The growth of algae has
been shown to be inhibited, and subsequently, the biomass of this
marine primary producer was reduced (Zhang et al., 2017). Heter-
oaggregation was shown to trigger the overexpression of the sugar
biosynthesis pathways in microalgae (Lagarde et al., 2016). Micro-
plastics have also been widely reported to cause the physiological
activities of moving and burrowing to be defective in the lugworm
Arenicola marina, which plays an essential role in oxygenating
sediments and controlling ecosystem services (Green et al., 2016).
Furthermore, the energy assimilation of the lugworm was
compromised due to the suppressed feeding activity, and the faunal
diversity of the sediment habitats could be vulnerable. As the prey
species for fish and wading birds, the function of secondary pro-
ducers may also be damaged during ecosystem nutrient cycling
(Wright et al., 2013b). As an emerging topic, the long-term or
ecological results have not yet been found, but such driving forces
for the disturbance of ecosystem productivity could result in al-
terations in biodiversity via defective development of species,
populations and communities.
5.2. Defective development of species, populations and
communities
The detrimental impacts of microplastics on the growth and
performance of individual organisms threaten the development of
the species and trophic-level energy transfer, leading to nonfunc-
tioning communities (Fig. 4.). The reduction in biodiversity trig-
gered by microplastics could also lead to defective community
development. The existence of microplastics at the nesting grounds
in the northern Gulf of Mexico altered the habitats of marine turtles
(including the temperature and permeability of the sediment),
which negatively affected the incubation of this endangered spe-
cies (Beckwith and Fuentes, 2018). Biodiversity contributes to the
ecological flexibility of ecosystems, and the interference in the lives
and reproduction of endangered species threatens their survival;
further loss of biodiversity could disturb the normal functioning of
ecosystems (Solan et al., 2004) (Fig. 5).
Moreover, a negative impact on individual organisms or single
species may be accumulated and magnified a disrupt community
10 H. Ma et al. / Environmental Pollution 261 (2020) 114089

Table 2
The combined effects of the inorganic and organic pollutants adsorbed on the surface of the microplastic.

Microplastic Pollutant Species Toxic effect Combination Effect Ref.

Inorganic Polystyrene/ Ni Daphnia Magna Abnormalities, including immobilization The acute toxicity test showed PS Kim et al.
Polystyrene-COOH and changes in morphology. exhibited a slight antagonistic effect on Ni (2017)
toxicity, whereas PS-COOH had a
synergistic effect with Ni.
Fluorescence red Hg European Accumulated the metal in the brain and Preadsorption for Hg on the microplastic Antao
polymer seabass muscles, causing neurotoxicity, oxidative accumulated the accumulation of Hg in Barboza
microspheres Dicentrarchus stress and damage, and changes in the tissues. et al.
labrax activities of energy-related enzymes in (2018)
juveniles of this species.
Polystyrene Cu zebrafish Danio Accumulation in tissue and toxicity to guts MPs and natural organic matter Qiao et al.
rerio and liver. aggravated the accumulation and toxicity (2019a)
of Cu. The levels of malonaldehyde and
metallothionein were increased, and the
superoxide dismutase was decreased.
Polyethylene Ag rainbow trout Accumulated Ag between the four No disturbance effect on the accumulation Khan
Oncorhynchus intestinal compartments of the mucus et al.
mykiss layer, mucosal epithelium, muscle layer, (2017)
and serosa.
Polyethylene Polychlorinated Lugworm Bioaccumulation and influence feeding Microplastic contributed marginally to Besseling
biphenyls (PCBs) Arenicola activity bioaccumulation. et al.
marina (L.) (2017)
Polyvinyl chloride Chiral antidepressant Loach Accumulating in loach tissues and liver Microplastic facilitated the transfer and Qu, 2018
venlafaxine and its Misgurnus subcellular. bioaccumulation of contaminants to the
metabolite anguillicaudatus liver and postpone the contaminants
O- metabolism in organisms
desmethylvenlafaxine
(pharmaceuticals)
Organic Polyethylene Triclosan (TCS) Marine Bioaccumulation metabolic activity and Microplastic potentiates TCS-mediated Syberg
microbeads (MP) hydrophobic organic copepod mortality. toxicity due to the adsorption capacity. et al.
contaminants (HOC) Acartia tonsa (2017)
(Dana)
polyethylene (PE), Triclosan (TCS) Microalgae Toxicity of microplastics on microalgae Th Joint toxicity of TCS and microplastic Zhu et al.
polystyrene (PS), Skeletonema mainly resulted from physical damage, and was all antagonism, and the antagonistic (2019)
polyvinyl chloride costatum the triclosan showed inhibition effect on effects increased with the higher
(PVC), and PVC800 the growth of microalgae. adsorption capacity of triclosan
Red fluorescent Procainamide and marine Reduced growth rate and the chlorophyll Toxicological interaction with microplastic Prata
polymer doxycycline microalga concentration. increased the adverse toxic effect. et al.
microspheres (pharmaceuticals) Tetraselmis (2018)
chuii
Fluorescent POPs polycyclic Artemia nauplii Desorb in the intestine and transferred to Functioned as a vector to facilitate the Batel
microplastic aromatic hydrocarbon and zebrafish the intestinal epithelium and liver contaminant transfer at different trophic et al.
particles benzo[a]pyrene (BaP) levels (2016)
Polystyrene plastic 14C-phenanthrene Daphnia Magna Bioaccumulation of phenanthrene-derived The adsorption capacity enhances the Ma et al.
particles residues in daphnia body and inhibited the toxicity (2016)
dissipation and transformation of
phenanthrene in the medium.
Polyethylene (PE) Polycyclic Aromatic mussel Accumulation in hemolymph, gills and Adsorption elevate bioavailability and Avio et al.
Polystyrene (PS) Hydrocarbons (PAHs) Mytilus especially digestive tissues. Alterations of toxicological pathway of the chemicals (2015)
galloprovincialis immunological responses, lysosomal
compartment, peroxisomal proliferation,
antioxidant system, neurotoxic effects, the
onset of genotoxicity
Polyethylene (PE) PAHs/PCBs/PBDEs Japanese e Altered the functioning of the endocrine Rochman
medaka Oryzias system in aquatic animal et al.
latipes (2014)
Polyethylene (PE) Benzo[a]pyrene Fish cell line Virgin industrial microplastic extract has no Benzo[a]pyrene coated extracts increase
Polypropylene toxic effect on fish cell line EROD activity and DNA damage
(PP)

development. Labeled microplastics ingested by zooplankton were
subsequently found in a mysid intestine, which showed the transfer
of microplastics from one trophic level (mesozooplankton) to a
higher level (macrozooplankton) (Set€ € et al., 2014). Mytilus edulis
ala
mussels were exposed to microplastics and experienced bio-
accumulation and biomagnification; the mussels were then fed to
Carcinus maenas crabs, which also displayed bioaccumulation and
biomagnification (Farrell and Nelson, 2013). Such trophic transfer
could disturb the flow of energy in the food web and the ecosystem.
In addition, even without direct impacts on one specific species,
microplastics may still be detrimental for interspecies interactions
(e.g., mutualistic relationship), which could cause a series of
cascading effects in aquatic ecosystems. For example, the damage
to European flat oysters Ostrea edulis was limited; the associated
benthic accumulation structures, however, were altered by micro-
plastic exposure, and the species abundance and the total number
of organisms were decreased by ~1.2 and 1.5 times, respectively
(Green, 2016).
5.3. Microcosm interference
Microorganisms, which constitute more than 90% of the living
 H. Ma et al. / Environmental Pollution 261 (2020) 114089 11

Fig. 4. The overall framework for the toxicological mechanism and the ecological implication: the microplastic enters the marine food chain and transfers throughout the different
trophic levels; the environmental pollutants adsorb on the microplastics or the plastic additives and are released after ingestion; the widespread microplastics affect the individuals,
then the population, before finally disturbing the community structure and function.

Fig. 5. The result microplastic toxicity on ecology.

biomass in the ocean, dominate the abundance, diversity and
metabolic activity in marine ecosystems. Because microorganisms
decompose marine organic matter, the variation in microbial
biomass and assemblages could change the carbon flux patterns
and the carbon-nitrogen cycle and modify the ecosystem function
(Fukuda et al., 1998; Azam and Malfatti, 2007). Compared to
autochthonous substrates, the longer half-lives and hydrophobic
surfaces of microplastics promote strong affinities with microor-
ganisms, which facilitates microbial interaction, colonization and
biofilm formation. After bacterial colonization of this enduring
habitat, plastisphere-specific bacterial assemblages with distinct
taxonomic compositions from the ambient environment develop
12 H. Ma et al. / Environmental Pollution 261 (2020) 114089
rapidly (Rummel et al., 2017; Zettler et al., 2013). The colonization
on microplastics alters the ecological function and the functioning
of microbial communities (Arias-Andres et al., 2018a). In a simu-
lation of the elevated levels of nutrients and the persistence of
substrates, the functional diversity and biomass of the microor-
ganisms were affected due to changes in the heterotrophic activ-
ities on the microplastics, which has potential impacts on global
bacteria-driven ecosystem processes such as C and N cycling
(McCormick et al., 2014). Moreover, the transfer frequency of
plasmids carrying antibiotic resistance genes was found to be
higher in the microplastic-associated bacteria compared to the
free-living bacteria, leading to microcosm interference via evolu-
tionary changes at the species and population levels (Arias-Andres
et al., 2018b).
Another issue with the interference of microplastics with mi-
crocosms is that some plastisphere members may be adaptable
pathogens. The Arenicola atlantica gut pathogens were detected on
microplastics after the excretion; the ingestion of microplastics by
organisms is inevitable, and the bacterial assemblages would be
changed after passing through the digestive tract (Kesy et al., 2016).
The occurrence of the human pathogens Vibrio spp. on marine
microplastics suggests that microplastics act as vehicles for multi-
trophic level transfer of pathogenic microorganisms (Kirstein et al.,
2016). Aeromonas salmonicaida, one of the most harmful invasive
bacteria responsible for infections in the fish, was recently found on
microplastics. The presence of A. salmonicaida has rarely been
recorded in the sea, but with the microplastics serving as vectors,
such pathogens may travel long distances and spread diseases on a
global scale (Virsek, 2017).
5.4. Vulnerable specific aquatic ecosystem
The prevalence of microplastics in ecosystems with unique
geographical characteristics as well as indispensable functions (e.g.,
wetlands, estuaries, mangroves, and deep ocean seafloor ecosys-
tems) presents a higher risk of deteriorating the vulnerable aquatic
environments. Therefore, the microplastic disturbances in highly
sensitive ecosystems should be highlighted.
The intertidal zone, which connects terrestrial and aquatic
ecosystems, is exposed to a high risk of influence from micro-
plastics due to its proximity to plastic debris sources. Microplastic
fibers were detected in the intertidal ecosystem of one exposed
beach and two protected beaches along the eastern shore of Nova
Scotia (Mathalon and Hill, 2014). The highest microplastic con-
centration occurred at the high tide line on the exposed beach
because the low-density microplastic debris is more likely to be
stranded at the upper limits of the wave action in this high-energy
environment. For the protected beaches, the highest microplastic
accumulation occurred in the low tide region due to the enhanced
deposition by the reduced waves and the altered properties of the
microplastics due to microbial films. The internal ecosystems were
exposed to both air and seawater and a high diversity of species
were exposed to heightened risk, which may present unexpected
impacts on both terrestrial and aquatic ecosystems (Mathalon and
Hill, 2014). Prior to the transfer of water to the marine ecosystem,
estuaries create “brackish” waters by mixing the freshwater from
river and saltwater from the ocean; these areas have also been
proven to be hotspots of microplastic contamination (Naidoo et al.,
2015; Sruthy and Ramasamy, 2017). The widespread microplastics
in the estuaries and wetlands of southern Europe and western
Africa have been detected in sediment samples, macro-
invertebrates, and shorebird feces, indicating that the microplastics
have entered into the food chain and show evidence of transferring
to the secondary intertidal consumers (Lourenco et al., 2017).
Another valuable ecosystem located between the land and the
ocean is the mangrove forest, which transports nutrients from the
land to estuaries and supports essential ecological functions (e.g.,
intercepting land-driven nutrients, pollutants, and suspended
matter from travelling to deeper water; exporting materials for
near-shore food webs; and buffering against natural hazards) (Li
et al., 2019; Valiela et al., 2001). The prevalence of microplastics
in this ecosystem was identified in seven intertidal mangrove
habitats in Singapore (up to three times higher than the concen-
trations reported in the UK) due to the degradation of marine
plastic debris. The interference of microplastics may hinder
mangrove ecological system functions and reduce ecosystem ser-
vices for coastal protection (Nor and Obbard, 2014).
Moreover, the invasion of microplastics into unknown regions is
no longer the most astonishing discovery. For instance, the deep sea
is considered as a major sink for the microplastics (Woodall et al.,
2014). Microplastics were first detected in pristine deep ocean
sediments worldwide in the polar front, Porcupine Abyssal Plain,
distal lobe of Congo Canyon, and Nile deep-sea Fan, indicating the
spread of microplastics throughout the unknown deep-sea regions
(Van Cauwenberghe et al., 2013). After these findings, widespread
microplastics (42e6595 microplastic/kg) were detected in Arctic
sea sediments at 2340e5570 m depths. The accumulation and
transport of microplastics may be attributed to sinking algal ag-
gregates and thermohaline circulation (Zhang et al., 2017;
Bergmann et al., 2017).
Marine snow is another transport vehicle for microplastics into
the abyssal depths of the ocean. The sink rate for microplastics was
shown to change significantly with incorporation into the snow,
changing from 818 m/day for the buoyant polymer polyethylene to
916 m/day for the denser polyamide fragments, which increased
the bioavailability to benthic organisms (Porter et al., 2018). After
identifying microplastics in the deep sea (>2200 m) at Rockall
Trough, North Atlantic Ocean, the microplastics were observed
being ingested by benthic macroinvertebrates through various
feeding modes (Courtene-Jones et al., 2017b). A True’s beaked
whale Mesoplodon mirus stranded on the coast of Ireland was
analyzed to study the ecology of the deep diving oceanic cetaceans,
and microplastics were found in the whale’s stomach (Lusher et al.,
2015). As the largest yet least studied ecosystem on earth, the
ecological function and structure of the vulnerable deep sea region
may be altered by anthropogenic pressure (Ahnert and Borowski,
2000; Puig et al., 2012).
Likewise, for the Arctic aquatic ecosystem, microplastics were
detected in particularly high concentrations in the sea ice at Fram
Strait, the Barents Sea slope, and even in the remote Central Arctic
(Peeken et al., 2018). Considering global climate change and the
yearly sea ice melt of between 1.6  104 km3 and 1.93  104 km3,
the potential release of microplastics was predicted at a minimum
of 7.2  1020 and a maximum of 8.7  1020 particles/year between
2011 and 2016. The variation in the microplastic pattern is prone to
occur in areas with strong seasonal sea ice melt or outflow
gateways.
6. The contradictory opinions about microplastic toxicity &
future research perspectives
The risk of microplastic toxicity has been the subject of a long-
standing debate. The main reasons that researchers have doubted
the environmental risks of microplastics are as follows:
1) The unrealistically high concentrations used during most
experiments;
2) The incomparable sampling and analytical approaches used;
3) The failure to provide solid evidence for the toxicity effect and
the dosage-effect response in different studies.
 H. Ma et al. / Environmental Pollution 261 (2020) 114089
For example, Kokalj et al. reported that facial cleanser micro-
plastic particles were not severely hazardous to isopods (Kokalj
et al., 2018b). Hermsen et al. suggest that the toxicity of the
microplastics presented in the environment might be lower than
anticipated due to the asymmetrical approach conducted during
the study (Hermsen et al., 2017). Limited acute toxicity was
observed from the ingestion of microplastics by the Antarctic krill
Euphausia superba, and no mortality or the dose-dependent weight
loss was observed; microplastics were eliminated by most of the
individuals without obvious bioaccumulation (Dawson et al., 2018).
Rehse et al. proposed that instead of accelerating, the microplastics
reduced the short-term effects of the environmental contaminant
bisphenol A (BPA) and polycyclic aromatic hydrocarbons by
adsorbing and lowering the concentrations of the residual con-
taminants to which the zooplankton Daphnia magna and microor-
ganisms were exposed (Rehse et al., 2018; Kleinteich et al., 2018). It
was even pointed out that the penchant for visibility, the pressure
to publish, the inability to publish negative results, the need for
funding, and sensationalism might have stimulated the exaggera-
tion of microplastics research (Burton, 2017).
Nevertheless, studies that unable to provide visible acute
toxicity evidence could not discount the possibility of long-term
chronic environmental disturbance when considering the ubiq-
uity and persistence of microplastics. As an emerging topic, the
different obscure microplastic-induced impacts could be easily
overlooked. For instance, one study found no evidence of increased
mortality, impacted reproductive parameters or morphological
changes in the water flea Daphnia magna (Imhof et al., 2017);
however, further observation revealed the alteration of gene
expression as a stress response. Additionally, nonlethal effects and
reproductive interference were observed in Hydra attenuata, and
disruption of feeding behaviors and changes to morphology were
observed that were certainly caused by microplastics (Murphy and
Quinn, 2018). On the one hand, the transfer of PCBs from micro-
plastics under simulated gut fluid conditions is fully biphasic and
reversible, even decreasing the bioavailability of the chemicals
present in the gut (Mohamed Nor and Koelmans, 2019). On the
other hand, the ingestion of microplastics enhances the PAH bio-
magnification due to the reduction in the fraction of PAHs available
for metabolization (Diepens and Koelmans, 2018). Organisms have
been shown to respond to microplastic toxicity in minor and
diverse ways, and the complexity of the actual environment and the
insufficient consideration by unsound studies could lead to ambi-
tious conclusions.
With decades of work, more research has started to conduct
experiments with environmentally relevant parameters (Lo €nnstedt
and Eklo€v, 2016), and attempts have also been made to determine
the true environmentally relevant toxicity by analyzing the
microplastic debris from the susceptible organisms stranded on
beaches (Lusher et al., 2015). The potential impacts of microplastics
on organisms and the environment had been revealed gradually,
and the possibility for transfer among different trophic levels and
food webs has been studied and confirmed (Set€ € et al., 2014;
ala
Farrell and Nelson, 2013). Without a better understanding of the
ecological consequences triggered by microplastics, it may not be
urgent to push the government to implement harsh bans on the use
of microbeads; however, intense management of microplastic
contamination should be encouraged.
For now, the interference of microplastics may appear to be an
unimpressive “minor disease” for the aquatic ecosystem: irritating,
yet with unclear and nondestructive consequences. The insufficient
attention paid may eventually make this issue more serious; when
the occurrence of severe consequences appears to be solid, we will
owe the future generation an explanation for why we neglected
13
this problem. Several reviews have discussed and explained that
microplastics present no risk to the aquatic environment (Adam
et al., 2018; Besseling et al., 2018; Burns et al., 2018), and the
attention from different perspective during this debate should be
regarded as an opportunity to broaden the collective knowledge
and should encourage researchers to further advance the toxico-
logical studies of microplastics. Therefore, we further emphasize
the significance of studying microplastic contamination of different
biota in various environmental settings. Researchers should
consider focusing not only on the identification of the effects on the
specific species but also on the broader ecological implications of
the effects of microplastics. Based on decades of microplastic
toxicological studies and the shortcomings discussed, the following
perspectives are suggested for future research:
1) Instead of presenting the common physiological parameters of
microplastics and the response of organisms generally, the
comprehensive consideration of the potential impacts should be
considered based on the features of the microplastics and the
behavioral and biological characteristics of organisms.
2) Multiple species of organisms and types of microplastics should
be used for toxicological risk assessments, and not only the
acute toxicity but also the sublethal chronic endpoints and the
ecotoxicological investigations at different trophic levels should
be considered further.
3) A database of the microplastic toxicity for different biota should
be developed systematically, and the adaptability of the existing
toxicological analysis models for microplastics should be tested.
4) The joint toxicity with environmental contaminants and the
long-term ecological consequences should be further
investigated.
5) Standardized methodology for the analysis of microplastic
contamination and toxicology should be regulated, and a par-
allel comparison with different research should be conducted to
advance the understanding of the general toxicity pattern of
microplastics.
The present review not only presented an overview introduc-
tion for all researchers investigating of the potential impacts of
microplastics but also provided a framework for researchers to
complete their work more systematically.
Declaration of competing interest
The authors declare that there is no conflict of interests
regarding the publication of this paper.
Acknowledgments
This work was supported by the National Natural Science
Foundation of China (41772264) and the Research Fund of State Key
Laboratory of Geohazard Prevention and Geoenvironment Protec-
tion (SKLGP2018Z001).
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