Ecotoxicology and Environmental Safety 217 (2021) 112243

Contents lists available at ScienceDirect

Ecotoxicology and Environmental Safety

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

Review

Effects of microplastics on marine copepods

Zhuoan Bai, Nan Wang, Minghua Wang *, 1
Fujian Provincial Key Laboratory for Coastal Ecology and Environmental Studies/College of the Environment & Ecology, Xiamen University, Xiamen 361102, China

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

Edited by: Dr Fernando Barbosa Microplastic contamination has been considered as a global environmental problem in marine ecosystem. Due to
small size (< 5 mm) in overlapping with that of microalgae, microplastics can easily be ingested by a wide range
Keywords: of marine copepods both in the laboratory and in situ. Although many studies have reported adverse effects of
Copepods microplastics on marine copepods, it still lacks a systematic overview about the bioavailability of microplastics
Microplastics
and their potential ecological consequences. As copepods dominate zooplankton biomass and provide an
Multigenerational exposure
essential trophic link in marine ecosystem, this review indicates the bioavailability and toxicity of microplastics
Toxicity
Vector in such taxon depend on the shape, size, abundance, and properties of plastics. Also, ours is purposed to tease out
the possible molecular mechanisms behind. Microplastic ingestion is prevalent; they impede food intake, block
the digestive tract, and cause physiological stress in copepods (e.g., immune responses, metabolism disorders,
energy depletion, behavioral alterations, growth retardation, and reproduction disturbance). Notably, in
response to microplastic exposure, the copepods show both species- and stage-specificity. Furthermore, micro­
plastics can serve as vectors of organic contaminants (e.g., triclosan, chlorpyrifos, and dibutyl phthalate) and
thus increase their toxicity in marine copepods, consequently aggravating the adverse impacts of microplastics in
marine ecosystem. Given that most previous studies have partially used pristine microplastics and their short-
term exposure might have undervalued their negative effects, more multigenerational mechanistic researches
(for example, via an integration of omics-based technology and phenotypic trait analysis) are urgently required
for numerous marine copepods exposed to environmental-characteristics plastics as demonstrated by aged
microplastics at environmentally realistic concentrations and added with other environmental pollutants; thus it
will not only provide mechanistic insights into the biological impacts of microplastics, but also help make the
seawater-benchmark setting and ecological assessment for microplastic pollution in marine environment.

1. Introduction
Due to human activities, a huge mass of plastic waste is annually
produced and finally imported into the global marine environment (for
example, via river input). For this reason, there has been more than 5
trillion plastic debris with over 250,000 tons floating in the global
oceans (Eriksen et al., 2014). In the marine environment, because of
several abiotic processes such as ultraviolet (UV) radiation and me­
chanical wear, plastics will eventually become small fragments, fibers or
granules with particle size < 5 mm, that is, "microplastics" (Hidalgo-Ruz
et al., 2012; Lusher et al., 2013). Conspicuously, at least 14.9 trillion
microplastic particles (weighing 93,300 tons) have been reported to be
afloat at the sea (Van Sebille et al., 2015). Furthermore, under the
business-as-usual scenario, the cumulative mass of plastic waste released
into the marine environment will be enhanced by an order of magnitude
by 2025 (Jambeck et al., 2015). Given the continuous increase in plastic
production and the stability of microplastics (for example, being
persistent for hundreds to thousands of years) in situ, the number of
microplastics will be increased but their average size will become
smaller in the ocean (Jahnke et al., 2017), rendering microplastic
contamination a more threat to marine ecosystem. Microplastics can be
divided into two major categories (Jahnke et al., 2017; Law, 2017). One
is primary microplastics and they are specially produced into small-size
plastics as microbeads in personal care products, textiles, and hygiene,
etc. The other is secondary microplastics, which come from break-down
of large plastics, for example, due to UV radiation and mechanical
wearing (Jahnke et al., 2017; Wright et al., 2013). Once in the ocean,
both primary and secondary microplastics can be ingested by numerous
marine animals including copepods (Cole et al., 2013; Desforges et al.,
2015; Fueser et al., 2020), mussels (Browne et al., 2008), oysters

* Corresponding author.
E-mail addresses: 616815530@qq.com (Z. Bai), 1053481977@qq.com (N. Wang), mhwang45@xmu.edu.cn (M. Wang).
1
Present address: Xiamen University, Xiamen 361102, China.

https://doi.org/10.1016/j.ecoenv.2021.112243
Received 13 December 2020; Received in revised form 1 April 2021; Accepted 3 April 2021
Available online 27 April 2021
0147-6513/© 2021 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Z. Bai et al. Ecotoxicology and Environmental Safety 217 (2021) 112243

Table 1
Microplastic effects and their bioavailability in marine copepods.
Species Microplastics Main findings References

Type Size (μm) Concentration

Acartia clause Fluorescent polystyrene 0.4-30.6 635-1×106 beads/ - The copepods show evidence of size-based selectivity. Cole et al. (2013)
Calanus beads mL - Copepods egest faecal pellets laden with microplastics.
helgolandicus - Exposure to 7.3-μm microplastics (> 4000 beads/mL)
Centropages typicus significantly decreases algal feeding.
Temora longicornis
Acartia tonsa Polystyrene beads, 20, 20×10, 80 microplastics/mL - The shape effects microplastic bioavailability to different Botterell et al. (2020)
Calanus fibers, and fragments and ≤20 species of copepods.
helgolandicus - The presence of the infochemical dimethyl sulfide can lead to
significant increases in the ingestion rate of microplastics in
copepods.
Acartia spp. Fluorescent polystyrene 10 1×103, 2×103 or - Ingested microsphere depends on different concentrations. Setälä et al. (2014)
Eurytemora affinis microspheres 1×104 particles/mL - E. affinis egests microspheres after 12-h.
Limnocalanus
macrurus
Calanus finmarchicus Nylon microplastic 10-30 or 50 microplastics/mL - Exposure to nylon fibers significantly decreases (average Cole et al. (2019)
granules or fibers 10×30 40%) the algal ingestion rates by C. finmarchicus, while no
difference is observed for nylon granules.
- C. finmarchicus exposed to nylon microplastics moult
significantly earlier than those in the control.
Calanus finmarchicus Polyethylene spheres 20 200 and 2000 - Microplastics did not affect fecal pellet production rate on Rodríguez-Torres
Calanus glacialis microplastics/L copepods. et al. (2020)
Calanus hyperboreus - Microplastic exposure caused stress-induced spawning in
copepods.
Calanus finmarchicus Polystyrene beads 15 and 30 50-200 beads/ - Both A. longiremis and C. finmarchicus can ingest Vroom et al. (2017)
Pseudocalanus spp. Polystyrene fragments ≤30 fragments/mL microplastics, A. longiremis only grazes the smaller (15-μm)
Acartia longiremis particles and C. finmarchicus for the two sizes, while
Pseudocalanus spp. cannot ingest any microplastics in such
case.
- Copepods ingest more aged microplastics than the pristine
one.
Calanus Fluorescent PE 10-32 100 microplastics/ - Exposed to microplastic fibers has a more pronounced impact Coppock et al.
helgolandicus microspheres mL on the copepods’ feeding than fragments. (2019)
Nylon fibers - Faeces containing low-density polyethylene descend signifi­
Polyethylene cantly more slowly than controls, but the sinking rates
terephthalate fibers significantly increase when high-density microplastics are
Nylon fragments incorporated within the faecal pellets.
Calanus Polystyrene beads 20 75 microplastics/mL - Microbead exposure significantly decreases the ingestion of Cole et al. (2015)
helgolandicus algal cells and carbon biomass in C. helgolandicus by 89% and
60%, respectively.
- Prolonged exposure to polystyrene beads significantly
decreases reproductive output, but the egg production rates,
respiration, and survival are negligibly affected.
Paracyclopina nana Polystyrene microbeads 0.05, 0.5, 6 10 μg/mL - The 0.05-μm beads can spread throughout the body of Jeong et al. (2017)
P. nana while the other two sizes are mostly distributed in the
digestive organs.
- The 0.05-μm nanobeads show a more prolonged retention
time in the body when compared with the other two sizes
(0.5- and 6-μm).
- Microplastics induce oxidative stress in the copepods.
Parvocalanus Polyethylene 5-10 1×104–8×104 - After 5-d of exposure to microplastics, egg production is Heindler et al.
crassirostris terephthalate particles/mL reduced in a dose-dependent manner. (2017)
- Exposure to microparticles (2×104 plastics/mL) for 6-d de­
creases the population size by 75% in contrast to the control,
while populations exposed for prolonged time with 24-d have
more severe depletions (i.e., 60% of control).
Pseudodiaptomus Monodisperse 0.5, 2, and 20, 200, and 2×103 - P. annandalei ingested three sizes of microplastics. Cheng et al. (2020)
annandalei polystyrene 10 μg/L - The intake of 0.5 and 2-μm microplastics was higher than
microspheres that of 10-μm microplastics.
- Microplastics were egested by P. annandalei through fecal
pellets.
Temora Turbinata Polystyrene microbeads 20 100 and 1×103 - The swimming behavior of copepod is significantly affected Suwaki et al. (2020)
(Dana, 1849) beads/mL by microbeads.
Tigriopus fulvus Polyethylene 1-5 0-1-10 mg/L - Microplastics can be transferred from copepods to jellyfish Costa et al. (2020)
nauplii microplastics ephyryae in the marine environment.
11
Tigriopus japonicus Polystyrene microbeads 0.05, 9.1×10 particles/ - Exposure to 0.5- and 6-μm polystyrene microbeads Lee et al. (2013)
mL significantly decreases the fecundity at concentrations (1.25-
0.5, 9.1×108 particles/ 25 mg/L) when compared with the control, but the 0.05-μm
mL PS nanobeads have no impact on such trait.
6 5.25×105 particles/
mL
Tigriopus japonicus Polystyrene beads 6 0.023 and 0.23 mg/L - Microplastics (0.23 mg/L) resulted in the significant Zhang et al. (2019)
reduction in survival rate, number of nauplii/clutch, and
fecundity.
(continued on next page)

2
Z. Bai et al.
Table 1 (continued )
Species Microplastics
Type Size (μm) Concentration
Tigriopus japonicus Polystyrene microbeads 0.05 and 20 mg/L
10
Tigriopus japonicus Polyethylene and 10-30 and 0,12.5, 25,
polyamide-nylon 6 5-20 50,100,200, and 400
microplastics mg/L
(Sussarellu et al., 2016), decapod crustaceans (Murray and Cowie,
2011), and fish (Boerger et al., 2010), potentially giving rise to negative
impacts in marine ecosystem.
In the environment, microplastics can serve as vector of toxicants to
marine organisms (Mei et al., 2020; Naqash et al., 2020; Rodrigues et al.,
2019). Firstly, the so-called additives are incorporated into plastics
during production so as to improve its properties, and these chemicals
will leach out of weathered plastic debris; please note that many addi­
tives have endocrine disruptor activity and can lead to detrimental ef­
fects in marine biota (Gunaalan et al., 2020). Secondly, microplastics
may sorb some hazardous compounds such as persistent organic pol­
lutants (POPs) and metals due to their large surface area-to-volume ratio
and hydrophobicity (Naqash et al., 2020; Rodrigues et al., 2019).
Collectively, regarding the ingestion of microplastics by marine animals,
the incorporated compounds during plastic production or sorbed
chemicals in situ can be accumulated in the biological tissues, producing
toxic effects in marine organisms at different trophic levels.
The interaction between marine organisms and microplastics de­
pends on the possibility of that organism encountering the microplastic
particles in the ocean, as well as the susceptibility of that species if their
interaction is occurring (Engler, 2012; Setälä et al., 2014). According to
patterns of ocean currents and biological productivity, the overlap of
marine organisms and microplastics is most likely to occur in shelf sea
regions (Clark et al., 2016); in these areas, marine copepods are
frequently found in huge abundance and have high probability to ingest
the microplastics. Marine copepods (the dominant members of
zooplankton community) have a crucial niche in marine ecosystem
because they consume primary producers (for example, phytoplankton)
and transfer the energy to higher trophic levels. Also, the copepods have
potential effects on biological pump because they can excrete feces for
carbon export to deeper-seawater or coprophagous biota in marine
environment (Cole et al., 2016). As marine copepods can ingest micro­
plastics with a size range similar to their preys (i.e., microalgae), accu­
rate predictions of microplastic effects in these organisms are pivotal to
better understand how marine ecosystem will respond to microplastic
contamination. Actually, several studies have demonstrated that
microplastic exposure can negatively affect the important life traits (e.g.,
growth and reproduction) in many copepods including Paracyclopina
nana (Jeong et al., 2017), Calanus finmarchicus, Pseudocalanus spp.,
Acartia longiremis (Vroom et al., 2017), and Tigriopus japonicus (Zhang
et al., 2019).
We present this particular and single-species review because,
whereas the effects of microplastics on marine biota (Botterell et al.,
2019; Wesch et al., 2016; Wright et al., 2013), and even the interactions
between microplastics and the chemicals (e.g., organic compounds,
metals, and POPs) (Mei et al., 2020; Naqash et al., 2020; Rodrigues et al.,
2019) have been widely reported, a specific and in-depth review about
the response of a single but vitally-ecological marine species in response
to microplastics is still very scarce. Given the species-specific response of
marine organisms in against microplastic contamination, and the
3
Ecotoxicology and Environmental Safety 217 (2021) 112243
Main findings References
- The two-generational effect of microplastics in copepods had
significant transgenerational proteome plasticity.
- Microplastic intake of both sizes gives rise to over-production Choi et al. (2020)
of reactive oxygen species and the antioxidant system is also
significantly affected.
- Microplastics had toxic effect on feeding, fecundity, and Yu et al. (2020)
survival in T. japonicus.
- Microplastics not significantly affected the body size of
T. japonicus in one generation time.
particularly crucial niche of marine copepods in the environment, the
occurrence and potential impacts of microplastics in the copepods
deserve special attention. Correspondingly, in this review, we have
summarized the bioavailability and effects of microplastics in different
copepod species and also discussed the possible molecular mechanisms
behind. Taken together, our purpose is more insightful into the micro­
plastic impacts in marine copepods, providing a basic framework for the
potential long-term ecological threats of microplastics to marine
ecosystem.
2. Method
The literatures were retrieved by Web of Science and Google Scholar
using a combination of keywords including "microplastic(s)", "plastic",
"zooplankton" and "copepod". The searched literatures were examined
individually and selected according to the copepod species and marine
system. Searches were performed until October 2020. The retained
publications are listed in Tables 1 and 2.
3. Microplastics in marine system
Plastics are ubiquitously present in marine environment and
constitute 80–85% of marine litters. Estimates suggest that 92% (~ 5.25
trillion) of plastic particles floating on the ocean surface are micro­
plastics (Auta et al., 2017; Eriksen et al., 2014). Consequently, marine
biota especially zooplankton are seriously threatened by microplastic
contamination. Microplastics enter the marine environment through
different pathways (manufacture & use, lake & river, and agriculture
land) as shown in Fig. 1. They are widely distributed in the water column
(please note that most will be retained in superficial seawater), sea floor,
marine sediments and beaches, and thus accumulated in marine biota of
different trophic levels (Ma et al., 2020). Marine microplastics are
available in various forms such as fibers, granules, beads and fragments
that differ in size, density, surface morphology, crystallinity, shape and
color (Hidalgo-Ruz et al., 2012). They are mainly composed of poly­
styrene (PS), polyvinyl chloride (PVC), and polyethylene terephthalate
(PET), which having specific gravity >1 are generally sinking in the
benthos, while polyethylene (PE) and polypropylene (PP) with specific
gravity <1 prefer to float on the surface (Andrady, 2011).
As stated above, there are two types of microplastics in marine
environment: primary and secondary (Jahnke et al., 2017; Law, 2017).
Primary microplastics (showing a microscopic size) are manufactured
for personal care products, textiles, and hygiene including facial
cleansers, toothpastes and pharmaceuticals. Remarkably, in numerous
researches, commercial microbeads (also known as virgin microplastics)
are frequently used and they can be considered as primary microplastics,
although this claim is controversial. Secondary microplastics are
breakdown of larger plastic debris under the physical, chemical or bio­
logical decomposition in situ (Andrady, 2011). Both primary and sec­
ondary microplastics are mainly floating on the ocean surface where the
Z. Bai et al. Ecotoxicology and Environmental Safety 217 (2021) 112243

plankton community occupies a major position, therefore increasing the

chances of being encountered and ingested by them (Fig. 1) (Cózar et al.,

Li et al. (2020)
Sørensen et al.

Bellas and Gil

Almeda et al.
Syberg et al.
2014). Collectively, microplastics will be expected to exist with high

Beiras et al.
References
quantity for long time and have potential threats on biological and

(2020)

(2017)

(2020)

(2019)

(2020)
ecological processes in marine ecosystem.

4. Bioavailability of microplastics to copepods

- Co-exposure to microplastics and oil pollution induced feeding suppression in C. hyperboreus.

- Microplastics insignificantly boost the accumulation and toxicity of two polycyclic aromatic
- C. finmarchicus can readily ingested polyethylene microbeads with an average size of 10-μm

- Presence of polyethylene microplastics doesn’t increase the bioaccumulation of 4-n-Nonyl­

diameter, but this copepod is not able to ingest microplastic particles of 100-μm diameter.

- Exposure to polyethylene microplastics can boost the toxicity of chlorpyrifos to copepods.

- Microplastics did not influence bioaccumulation of polycyclic aromatic hydrocarbon in

- The combined effect between microplastics and Dibutyl phthalate to the copepods was
The bioavailability of microplastics reflects the proportion of plastic
particles in the environment that can be uptaked by an organism; it
depends on several abiotic and biotic factors including the shape, size,
abundance and properties of microplastics, and selectivity of biota

phenol and 4-Methylbenzylidene-camphor and their toxicity in copepods.

(Wright et al., 2013), and all the above will modulate the effects of
microplastics in marine organisms. For example, ingestion of micro­
plastics by the copepods has shape- (Sun et al., 2018), species- (Vroom
et al., 2017) and/or stage-specificity (Lee et al., 2013), which will in turn
influence the biological impacts. In view of the important niche played
- Microplastics potentiate the acute toxicity of triclosan.

by the copepods in marine ecosystem, microplastic effects have been

- Microplastics can serve as a vector of chlorpyrifos.

studied intensively in this species (Tables 1 and 2), and it can help to
improve the ecological assessment and benchmark setting for micro­
plastic contamination in marine environment.

4.1. Shape

In the marine environment, microplastics are existing mainly in the

types of fibers, granules, beads and fragments (Hidalgo-Ruz et al., 2012).
The majority of laboratory studies has used microbeads/microspheres
for microplastic exposure, showing that they can be ingested by a
C. helgolandicus.
hydrocarbons.

antagonistic.

number of copepods including Acartia clause, Calanus helgolandicus,

Main findings

Centropages typicus, Temora longicornis (Cole et al., 2013), Acartia spp.,

Eurytemora affinis, Limnocalanus macrurus (Setälä et al., 2014), P. nana
(Jeong et al., 2017), Pseudodiaptomus annandalei (Cheng et al., 2020),
and T. japonicus (Zhang et al., 2019). Conversely, some field researches
Polycyclic aromatic hydrocarbon

investigating microplastic ingestion by marine copepods in the East

China Sea, Northern South China Sea, and North East Pacific have re­
Methylbenzylidene-camphor

ported that microfibers are the most commonly ingested in the envi­
ronment (Sun et al., 2017, 2018; Desforges et al., 2015). The possible
4-n-Nonylphenol, 4-
Polycyclic aromatic

reason may be that microfibers are more bioavailable in the copepods or

Dibutyl phthalate
Pollutant type

the highest rates of microfibers encountered by them is occurring in situ

hydrocarbons

Chlorpyrifos

by contrast to other shapes. In recent years, several studies have evi­

Triclosan

denced the selectivity and effects of differently-shaped microplastics in

marine copepods including C. helgolandicus (Coppock et al., 2019),
C. finmarchicus (Vroom et al., 2017) and A. tonsa (Botterell et al., 2020).
Combined effects of microplastics with other pollutants in marine copepods.

For instance, C. finmarchicus is exposed to two types of microplastics

0, 0.1, 1, 10 and 100

20, 50, 100, 200 and

20 microplastics/mL
7.5 × 104-2.7 × 108

(beads and fragments) so as to compare the ingestion of different

microplastic shapes by the copepods (Vroom et al., 2017). The results
Concentration

0.96 g/cm3
particles/L

1.33 g/mL

show that consumption of the beads by the individuals displays

500 mg/L

stage-specificity but it is not the case for fragments. Additionally, in

μg/L

adult females C. helgolandicus exposed to nylon fragments and fibers,

both shapes of nylon can be readily ingested, and the most commonly
ingested fiber size being 10 × 40 µm (Coppock et al., 2019).
Size (μm)

0.1, 0.55
10–200

In fact, ingesting differential microplastic shapes both under the

10–90

and 5
2–10

20.7
4–6

laboratory and in situ is prevalent for marine copepods (Coppock et al.,

2019; Jeong et al., 2017; Setälä et al., 2014; Suwaki et al., 2020), but the
exact causation is not clear. Botterell et al. (2020) investigated three PS
spherical particles

shapes (bead, fiber, and fragment) ingested by marine zooplankton

including two copepod species (C. helgolandicus and A. tonsa), and
Microplastics

microplastics

microplastics
Polyethylene

Polyethylene

Polyethylene

Polyethylene

Polyethylene
Polystyrene

Polystyrene
microbeads

microbeads

microbeads

revealed that the copepod’s species-specific ingestion on microplastics is

due to various shapes of plastics; for example, A. tonsa likes fibers while
Type

C. helgolandicus prefers to ingest fragments. They further attribute this

phenomenon to different feeding strategies of the copepod species, for
example, with particular plastic shapes being easier to handle, or some
helgolandicus
finmarchicus

Acartia clausi
Acartia tonsa

Acartia tonsa

Acartia tonsa

copepods having species-specific capacities to ingest (Botterell et al.,

japonicus
(Dana)

Tigriopus

2020).
Calanus

Calanus
Species
Table 2

Regardless of shapes consumed by marine copepods, besides the

chemical impact, microplastics could lead to physiological damage as

4
Z. Bai et al.
Manufacture & use
EDCs
Primary source
MPs
PCBs
PAHs
Epipelagic
Mesopelagic
Bathypelagic
Sea floor
Fig. 1. Sources and transport of microplastics as well as their biological impacts in the marine environment.
exemplified by digestive tract blockage, ultimately producing adverse
effects in the copepods (Choi et al., 2020; Cole et al., 2015; Jeong et al.,
2017). For example, the adult female C. helgolandicus can readily ingest
three different types/shapes of microplastics (fluorescent PE micro­
spheres, nylon fibers/fragments, and polyester fibers) after exposure,
and moreover, in contrast to the fragmented microplastics, exposed to
the fibers has a more pronounced impact on the copepods’ feeding,
resulting in their compromised fitness (Coppock et al., 2019). Addi­
tionally in the copepod C. helgolandicus, exposure to 20-μm PS beads
significantly reduces the algal ingestion (Cole et al., 2015). Analogously,
to investigate the effects of different microplastic shapes on the co­
pepod’s feeding activity, Cole et al. (2019) conducted a 3–4 day expo­
sure test using nylon fibers and granules; they discover that exposure to
nylon fibers significantly decreases (average 40%) the algal ingestion
rates of Scripsiella trochoidea (29 × 34 µm) and Thalassiosira rotula
(19 × 24 µm) by C. finmarchicus, while no difference is observed for
nylon granules.
Collectively, microplastic consumption by marine copepods appears
to be related with shapes of plastics, and it can be explained at least by
the probability of copepods encountering microplastics and their dif­
ferential feeding strategies (e.g., some copepods preferring to ingest
certain shapes of microplastics). Meanwhile, differential shapes of
microplastics may produce diverse eddies by interfering with predator-
prey currents, which can also affect the selectivity of copepods species
during plastic ingestion (Onink et al., 2019). Irrespective of varied
shapes, after consumption, microplastics will probably cause gut
blockage and reduced food intake, and it will ultimately produce a
compromised fitness in an individual marine copepod.
4.2. Size
As mentioned above, microplastics are described as plastic particles
< 5 mm in diameter and thus this class includes a wide range of sizes.
Whether or not the copepod species can ingest microplastics chiefly
depends on the size range and shape of its preferred preys as compared
with those of microplastics encountered by the copepods (Cole et al.,
2013; Setälä et al., 2014).
A recent field work has indicated that the size of microplastics
detected from the copepods in East China Sea primarily ranges from 21-
5
Ecotoxicology and Environmental Safety 217 (2021) 112243
UV radiation
Heavy metals
PBDEs
Secondary source
Mechanical wear
Wind scouring Plastics
μm (pellets) to 280-μm (fibers) (Sun et al., 2018). In the laboratory,
several copepods including C. typicus, T. longicornis, Acartia clausi and
C. helgolandicus can ingest the fluorescent PS beads with varying de­
grees: T. longicornis and C. typicus are able to ingest 7.3-, 20.6-, and
30.6-μm microbeads, whereas A. clausi and C. helgolandicus have mainly
consumed 7.3-μm microbeads (Cole et al., 2013). Additionally, Vroom
et al. (2017) selected two sizes (15- and 30-μm) of PS microbeads at a
concentration of 0.41 mg/L to measure microplastic consumption in
three copepods, i.e., C. finmarchicus, Pseudocalanus spp. and A. longiremis
under a 24-h exposure. The results show that consumption of PS beads is
dependent on species as well as plastic size; namely, although both
A. longiremis and C. finmarchicus can ingest microplastics, A. longiremis
only grazes the smaller (15 μm) particles and C. finmarchicus for the two
sizes; please note that Pseudocalanus spp. cannot ingest any micro­
plastics in such case (Vroom et al., 2017). An explanation is probably
that these two copepods (A. longiremis and C. finmarchicus) have
different body sizes; namely, the adults A. longiremis are 0.9–1.3 mm in
length and thus prone to ingest less microplastics than the latter
(2–4 mm) (Vroom et al., 2017). Taken together, the copepods are
confirmed to display size-specific responses in against microplastic
exposure, but the exact causation really deserves a further investigation.
Post-ingestion, the size of microplastics is also a crucial factor
determining the translocation ability of microplastics and adverse ef­
fects in marine copepods (Jeong et al., 2017; Lee et al., 2013). For
instance, P. nana has been demonstrated to ingest three different sizes
(0.05-, 0.5-, and 6 μm) of PS beads; and remarkably, after exposure, the
0.05 μm beads can spread throughout the body of P. nana while the
other two sizes are mostly distributed in the digestive organs (Jeong
et al., 2017). Additionally, they also find that the 0.05-μm nanobeads
show a more prolonged retention time in the body when compared with
the other two sizes (0.5- and 6 μm) (Jeong et al., 2017), suggesting that
smaller beads are more likely to remain in the copepods than larger
ones. For T. japonicus, exposure to 0.5- and 6 μm PS beads significantly
decreases the fecundity at concentrations (1.25–25 mg/L) by contrast to
the control, but the 0.05-μm PS beads have no impact on such trait (Lee
et al., 2013).
Z. Bai et al.
4.3. Age
Age is capable to influence the properties and fate of microplastics in
the marine environment by affecting their surface morphology and
microstructure, which will modulate the bioavailability and toxicity in
marine copepods (Jahnke et al., 2017). Most reported literatures have
used pristine microplastics to examine their effects in marine copepods
(Bellas and Gil, 2020; Cheng et al., 2020; Cole et al., 2019; Coppock
et al., 2019; Jeong et al., 2017), but they may have probably given
misleading information about the biological impacts of plastics in the
environment. So far as we have known, there has been only one previous
study investigating the effect of aged microplastics on the copepods
(Vroom et al., 2017). Namely, they compare the intake of pristine and
aged microplastics by the copepods of C. finmarchicus CV and
A. longiremis females, and find that the individuals ingest more aged
microplastics than the pristine (Vroom et al., 2017). As for the differ­
ential fate of pristine and aged microplastics in the copepods (Vroom
et al., 2017), three explanations are listed as follows. The first one is
attributed to the ability of many copepods to distinguish the quality of
food and choose natural rather than artificial particles (Cole et al., 2016;
Harrison et al., 2011). The second is due to biofilms which have been
shown to grow on pristine plastics in seawater within hours (Ober­
beckmann et al., 2015; Zettler et al., 2013), and the preference of two
copepods for aged microplastics is possibly ascribed to biofouling.
Meanwhile, biofilms can release chemical signals that alter the surface
properties of microplastics, rendering aged plastics more similar to food
items than pristine ones (Lobelle and Cunliffe, 2011). The third is the
density of microplastics; as the microplastics acquire biofilms, they will
become denser and therefore sink faster, making them attractive food
for zooplankton (Kooi et al., 2017).
Collectively, the information concerning the effects of aged micro­
plastics on marine copepods is very scare, but it is urgently important as
the use of pristine microplastics may probably underestimate their
biological impacts in marine ecosystem.
4.4. Abundance
Given that plastics can continually undergo degradation in marine
environment, the abundance of microplastics will be increased as the
size is decreasing, thus impacting their bioavailability. In the northern
part of South China Sea, Sun et al. (2017) found that the abundance of
microplastics ingested by copepods is 2.19 pieces/m3 on average if a
505 µm mesh net is used but 103.49 particles pieces/m3 for a 160 µm
net. Similarly, many laboratory studies have shown that higher con­
centration of microplastics can give rise to increased ingestion by marine
copepods and consequently result in differential biological effects
(Cheng et al., 2020; Heindler et al., 2017; Lee et al., 2013; Setälä et al.,
2014; Zhang et al., 2019). A dose-effect of microplastics (PET) on the egg
production and population size has been observed in the calanoid
copepod Parvocalanus crassirostris; for example, after 5 day exposure to
microplastics (1–8 × 104 particles/mL), the egg production rate is
decreased in a concentration-dependent mode (Heindler et al., 2017).
Also, our earlier study has investigated the effect of microplastics in
T. japonicus under multiple-generation exposure to two environmentally
relevant concentrations (0.023 and 0.23 mg/L; 6 μm PS microbeads):
the high (0.23 mg/L) microplastic exposure significantly compromises
the survival and reproduction of T. japonicus for two generations but low
treatment (0.023 mg/L) shows little influence; please note that the
average ingestion of microplastics by T. japonicus is calculated as 2 and
38 microbeads/individual, respectively, for the 0.023 and 0.23 mg/L
exposures (Zhang et al., 2019). Together, higher concen­
tration/abundance microplastics seem to display more negative impacts
in marine copepods.
Of particular note, the abundance for different shapes is also very
important to the bioavailability of microplastics in marine copepods as
such taxon has the shape-dependent ingestion (please refer to the
6
Ecotoxicology and Environmental Safety 217 (2021) 112243
detailed information in Section 4.1), and moreover, varied shapes have
differential concentrations in the environment (La Daana et al., 2017;
Lindeque et al., 2020; Sun et al., 2018; Zhang et al., 2020). Previous
studies have reported that fibers are the most prevalent in the Atlantic
Ocean (94%) (La Daana et al., 2017), mid-west Pacific Ocean (57.4%)
(Wang et al., 2020), and coastal waters of the Gulf of Maine, USA (84%)
and western English Channel, UK (77%) (Lindeque et al., 2020).
Differently, microplastics in Yellow Sea, China are mainly fragments,
accounting for 42%; the percentage of film, foam, and fiber is 22%, 19%,
and 16% respectively (Sun et al., 2018). In a recent study of the
spatio-temporal distribution of plastic and microplastic debris in the
surface water of Bohai Sea (China), they have collected the plastic debris
during four seasons of 2016–2017 and found that most plastic particles
are lines, fragments, foams, and fibers, respectively, contributing to
38%, 35%, 13%, and 12% (Zhang et al., 2020). Accordingly, the abun­
dance of differential plastic shapes in situ appears to link with the col­
lecting region, and the exact causation may be complicated than what
has been expected (please note that microplastic pollution is primarily
caused by tourism, agriculture, aquaculture, domestic and industrial
sewage, one of which can be the cause). Nevertheless, one thing we can
ascertain is that varied shapes may probably modulate the role by the
concentration/abundance of microplastics in the biological impact of
plastics, calling the urgent need to focus more on this issue.
5. Effect of microplastics on marine copepods
Many works have confirmed ingestion of microplastics by a wide
range of copepods both in the laboratory (Cheng et al., 2020; Cole et al.,
2013; Jeong et al., 2017; Vroom et al., 2017; Zhang et al., 2019) and in
situ (Sun et al., 2017, 2018) which include T. longicornis, C. typicus,
A. clausi, C. helgolandicus (Cole et al., 2013), P. nana (Jeong et al., 2017),
C. finmarchicus, Pseudocalanus spp., A. longiremis (Vroom et al., 2017),
T. japonicus (Zhang et al., 2019), and P. annandalei (Cheng et al., 2020).
The frequency and extent of microplastic ingestion are related to the
feeding strategy of copepods, as well as the shape, size and properties of
microplastics (Cole et al., 2013; Setälä et al., 2014). Marine copepods
primarily graze in surface waters that contain large amounts of micro­
plastics, increasing the chances of plastic exposure and its intake in the
individuals (Cózar et al., 2014). As microplastics are presented in a size
range similar to the copepod’s preys, they can readily be grazed by a
wide range of pelagic and benthic copepods, hence resulting in negative
effects from molecular response to an individual’s fitness such as
retarded growth and limited reproduction (Cole et al., 2015, 2013;
Jeong et al., 2017; Zhang et al., 2019).
5.1. Ingestion/egestion
As early as 1970s, some laboratory exposure researches have
discovered the ingestion of microplastics by copepods (Ayukai, 1987;
Wilson, 1973). In recent years, microplastic consumption has been
revisited in many copepods such as P. nana (Jeong et al., 2017),
C. helgolandicus (Coppock et al., 2019), T. japonicus (Zhang et al., 2019),
P. annandalei (Cheng et al., 2020), C. finmarchicus, and A. longiremis
(Vroom et al., 2017). Notably, the wild copepods from the South China
Sea (Sun et al., 2017), the East China Sea (Sun et al., 2018), and
Northeast Pacific Ocean (Desforges et al., 2015) have been reported to
readily consume microplastic fibers and particulates in the marine
environment. Of particular note is that microplastics can be transferred
from copepods to the higher trophic chain levels (e.g., jellyfish) as
microplastics are ingested in the jellyfish ephyryae (Aurelia sp.) after
feeding on the copepod nauplii (Tigriopus fulvus) contaminated with PE
microbeads (Costa et al., 2020), calling the potential that microplastics
can be transported at different trophic levels and ultimately to human
beings. Overall, due to the small size, abundance, and high persistence of
microplastics in the environment, it seems very usual that marine co­
pepods can easily ingest such plastics in situ, which will ultimately give
Z. Bai et al.
rise to adverse health effects in marine ecosystem.
Microplastic ingestion by copepods is both species and life stage
specific, besides the dependence on plastic size. Cole et al. (2019) re­
ported the nylon fibers and granules in the intestines and faeces of ju­
venile C. finmarchicus after two hours of exposure, confirming
microplastic ingestion/egestion. Similarly, three copepods
(C. finmarchicus, Pseudocalanus spp. and A. longiremis) are selected to
graze the PS beads of two sizes (15- and 30-μm) during a 24-h exposure,
demonstrating that the ingestion of PS beads depends on species as well
as plastic size; that is, both A. longiremis and C. finmarchicus have preyed
on the microplastics of two sizes, but Pseudocalanus spp. cannot perform
such grazing (Vroom et al., 2017). Meanwhile, after ingestion, the 15 μm
microbeads move peristaltically into the gut, which are collected in the
back intestine and excreted within a few hours (Vroom et al., 2017). A
study by Yu et al. (2020) shows that both PE and polyamide-nylon 6
microplastics can be ingested by T. japonicus, and thus have a
dose-dependent toxicity effect on the copepod’s fitness (e.g., feeding,
egestion, survival, and reproduction). In comparison, Outram et al.
(2020) have found no evidence of microplastic consumption by the
copepods T. longicornis in Chichester Harbor, United Kingdom although
microplastics are recorded in all water samples in this harbor; the au­
thors argue that this copepod species may probably perform selective
feeding and thus avoid to ingest microplastics in the environment.
However, some will challenge the above results because the small
sampling size (i.e., only ninety copepods) is collected for microplastic
examination, which also misses the plastic size lower than 23-μm, in this
study (Outram et al., 2020) and, as a consequence, provides misleading
information.
Cole et al. (2013) reported that several copepods common to the
northeast Atlantic have ingested fluorescent PS beads, with the capacity
to be uptaken varying among species, developmental stages, and
microplastic size. Post-ingestion, microbeads are usually accumulated in
the anterior midgut, shifted to the posterior midgut through peristaltic
action, and egested as fecal pellets (Cole et al., 2013). Please note that
the faecal packages of marine zooplankton including copepods can serve
as an important source of nutrients, carbon and energy for deeper-water
or coprophagous biota during their sinking, having the potential to
affect the biological pump as these pellets contribute to the vertical flux
of particulate organic matters in the ocean (Turner, 2015). Intriguingly,
a previous study shows that consumption of the PS microplastics has
significantly decreased the density of the faecal pellets excreted by the
copepod C. helgolandicus, which is capable to modulate their fate
(probably increasing their stay) in the water column; furthermore, this
research also indicates that microplastics which are incorporated into
the faeces of C. typicus can be ingested by and transferred to
C. helgolandicus (Cole et al., 2016), raising the potential that micro­
plastics have trophic bioavailability in the marine environment. More
interestingly, in another study, after microplastic intake by the copepod
C. helgolandicus, the sinking rates of faecal pellets are significantly
altered, and they primarily depend on the density of the polymer in the
faeces; for example, if the egests have low-density PE, they descend
more slowly than the controls, but the sinking rates are significantly
enhanced when high-density microplastics (i.e., PET) are incorporated
within the faecal pellets (Coppock et al., 2019). Although the above
researches have evidenced that microplastics can modulate the density
and/or sinking rates of faecal pellets from the copepods, some will doubt
about it. For example, three arctic copepods (C. finmarchicus, C. glacialis,
and C. hyperboreus) are acutely exposed to two concentrations of PE
microbeads (i.e., 200 and 20,000 plastics/L) under various food avail­
ability; the results indicate that microplastics insignificantly affect the
fecal pellet production rates in all copepod species, although the PE
beads are presented in the fecal pellets of each species (Rodríguez-Torres
et al., 2020). They also find that microplastic ingestion shows little
impact on the sinking rates in C. hyperboreus faeces (Rodríguez-Torres
et al., 2020).
7
Ecotoxicology and Environmental Safety 217 (2021) 112243
5.2. Feeding capacity
Recalling that microplastic ingestion is a common issue for the co­
pepods either under the laboratory-controlled condition or in the envi­
ronment, some researches will argue this may comprise their feeding
capacity and thus decrease the energy input as its ingestion has been
reported to cause physiological damages including gut blockage in the
alimentary tract in several marine animals (Choi et al., 2018; Espinosa
et al., 2019; Welden and Cowie, 2016). Indeed, numerous previous
works have showed that microplastic exposure is capable to repress the
copepod’s feeding activity (Cole et al., 2013, 2015, 2019; Coppock et al.,
2019). Taking an example, the copepod C. typicus is subjected to natural
algal assemblages with and without PS (7.3-μm) microbeads at a con­
centration > 4000 beads/mL, demonstrating that microplastic treatment
has significantly led to a reduced grazing upon algal cells (Cole et al.,
2013). In another work, ingestion of microplastics can also compromise
the copepod’s feeding activity; that is to say, exposure to 20-μm PS
microplastics (75 beads/mL) has decreased the ingestion of algal cells
and carbon biomass in C. helgolandicus by 89% and 60%, separately
(Cole et al., 2015). In particular, when C. helgolandicus is exposed to four
different sizes/shapes of microplastics, the exposure at a concentration
of ~100 plastics/mL can reduce the algal grazing and also cause a shift
in algal preference; for instance, exposed to nylon fibers remarkably
decreases the copepods’ grazing upon algae with similar size (i.e., Pro­
rocentrum micans) and shape (i.e., T. rotula), but such exposure insig­
nificantly affects the ingestion of Dunaliella tertiolecta (Coppock et al.,
2019). Similarly, in an ecologically-important cold water copepod
C. finmarchicus, exposure to the nylon microplastic fibers (10–30 µm;
~50 plastics/mL) has caused obvious shifts in the copepod’s feeding as
exemplified by significantly decreased ingestion rates for the largest
algae S. trochoidea (29 × 34 µm) and T. rotula (19 × 24 µm), conse­
quently giving rise to a 40% reduction in ingested biomass by compar­
ison with the controls (Cole et al., 2019). Remarkably, a recent work
shows that, after 24 h exposure, both 0.5- and 10-μm PS microplastics
significantly decrease (by approximately 50%) the filtration and inges­
tion rates of P. annandalei in relative to the control group (please note
that the copepods are supplied with microalgae Platymonas helgolandica
at 1 × 105 cells/mL), however, which are negligibly affected by the
2-μm microbeads (Cheng et al., 2020).
Overall, microplastics can modulate the feeding capacity such as
grazing rate and prey selection and thus alter the total energetic input
(primarily as demonstrated by energetic depletion) in the copepods,
which will reallocate the energy into some critical life traits including
growth and reproduction and ultimately compromise an individual
fitness.
5.3. Growth and reproduction
Recalling that microplastic presence can repress a marine in­
dividual’s feeding capability and decrease the total energetic input, its
consumption has expectedly and broadly compromised the growth/
reproduction of copepods in many previous researches (Cole et al., 2015;
Heindler et al., 2017; Jeong et al., 2017; Lee et al., 2013; Zhang et al.,
2019). Cole et al. (2015) discovered that the 9-day exposure to 20 μm PS
microplastics (75 plastics/mL) insignificantly affects the egg production
rate, oxygen consumption and survival in C. helgolandicus, but it can
significantly reduce the reproductive output as exemplified by decrease
in egg size and hatching success in the treated copepods; they further
argue that microplastic consumption can result in energetic shortage via
impeded algal grazing, consequently decreasing the copepod’s repro­
ductive performance. In the study of Heindler et al. (2017), the effects of
microplastics (PET) on the egg production and population size have
been examined for the calanoid copepod P. crassirostris. That is to say,
after 5 days of exposure to microplastics (1–8 × 104 particles/mL), egg
production is reduced in a concentration-dependent manner; in the
meantime, exposure to microparticles (2 × 104 plastics/mL) for 6 days
Z. Bai et al.
Microplastics
Size
Shape
Ingested
Concentration
Age
Faeces
Type
Carbon export
EDCs Heavy metals
PBDEs
MPs
PCBs
Biological pump
PAHs
Fig. 2. The bioavailability of microplastics and their effects in marine copepods.
decreases the population size by 75% in contrast to the control, while
populations exposed for prolonged time with 24 days have more severe
depletions (i.e., 60% of control) (Heindler et al., 2017). Regarding that
marine animals are frequently challenged with microplastic contami­
nation over many generation in the environment, a multigenerational
microplastic study is very important as it can mimic the real scenario
and thus display environmental relevance and significance. Neverthe­
less, so far as we have known, there are only two multigenerational
microplastic stress researches in marine copepod (Lee et al., 2013;
Zhang et al., 2019). The first has adopted a two-generation test to
investigate microplastic effect on the important life traits including
development and reproduction in the marine copepod T. japonicus; for
example, exposed to 0.5- and 6-μm PS microbeads has significantly
reduced the copepod’s fecundity of both generations at concentrations
(1.25–25 mg/L; in the case of 25 mg/L, 3.64 × 108 and 2.1 × 105
beads/mL are designated, respectively, for 0.5- and 6-μm PS micro­
plastics in seawater solutions) in relative to the control, which is prob­
ably attributed to depleted nutrition and inhibited fertilization caused
by ingestion of microbeads. Please note that the doses of microplastics
used in the above work are far more than those in the marine environ­
ment (Lee et al., 2013), hence embracing the urgent need to have
such-kind multigenerational researches at environmentally-realistic
concentrations. In this context, our earlier study is the first to investi­
gate the effect of microplastics on marine copepod under
multiple-generation exposure to environmentally-realistic concentra­
tions (0.023 and 0.23 mg/L 6 μm PS microbeads being equal to 194 and
1937 particles/mL respectively); that is, despite low exposure
(0.023 mg/L) displaying little effect, the 0.23 mg/L microplastic expo­
sure has significantly reduced the survival rate and reproductive capa­
bility of the copepods T. japonicus at two generations (Zhang et al.,
2019). Thus, microplastic presence can decrease a marine copepod in­
dividual’s growth and reproduction and, as a consequence, potentially
affect the population size and recruitment, ultimately posing a threat to
the structure and function of marine ecosystem.
6. Potential mechanisms concerning microplastic effect in
copepods
At the present moment, we know that microplastics can impede the
copepod’s feeding capacity and reduce the total energy input, conse­
quently decreasing the energetic reallocation into some critical life traits
as demonstrated by compromised growth/reproduction in the
Ecotoxicology and Environmental Safety 217 (2021) 112243
Biological effects
Oxidative damage
Subcellular
Immune response
Entangling feeding appendages
Blocking the alimentary canal
Decreasing algal ingestion Metabolism disorders
Cellular
Energy depletion
Inducing chemical effects
Reduced ingestion
Individual
Growth retardation
Ecosystem Fecundity
Population
function Population size
conditioned individuals due to the trade-off. Many studies have evi­
denced the microplastic-induced adverse effects in marine copepods,
which range from impede feeding capacity to physiological damages
(Choi et al., 2020; Cole et al., 2019; Lee et al., 2013). We summarize the
effects to establish a basic research framework for future microplastic
stress researches (Fig. 2). The adverse impacts of microplastics on co­
pepods are thought to primarily include physical damage and chemical
effect. The former is mainly related to the ingested microplastics being
capable to entangle feeding appendages and block the alimentary tract
in the stressed individuals, hence causing reduced feeding, malnutrition
and even death (Cole et al., 2013; Jeong et al., 2017; Zhang et al., 2019).
The other risk coming from the intake of plastics is attributed to its
inherent chemical nature (for example, the plastics normally contain
additives and some of them display endocrine disruption activity) and
large surface area-to-volume ratio which enables them to accumulate
POPs or metals (Wright et al., 2013); the consequence is that, after
consumption of microplastics, the incorporated or absorbed toxicants
can have damaging effects in marine copepods.
Although quite a few researches have indicated ingestion of micro­
plastics and its impact in marine copepods (Cole et al., 2013, 2015,
2019; Coppock et al., 2019; Lee et al., 2013; Vroom et al., 2017), very
scare information is available to elucidate the molecular mechanisms
behind (Choi et al., 2020; Jeong et al., 2017; Zhang et al., 2019). In the
pilot study of Jeong et al. (2017), accumulation of reactive oxygen
species (ROS) and induction of antioxidant enzymes (e.g., glutathione
peroxidase, superoxide dismutase, and glutathione-S-transferase) have
been reported in the marine copepod P. nana after exposure to different
sizes of PS microbeads, suggesting the microplastic-induced oxidative
stress in the exposed animals; they further investigate the pathways of
mitogen-activated proteins kinase (MAPK) and nuclear factor erythroid
2-related factors (Nrf2, acting as a downstream transcription factor of
MAPKs), and find that ROS over-production has increased phosphory­
lation of p38 and ERK and subsequently resulted in activation of Nrf2. It
should be noted that the Nrf2 activation can induce expression of anti­
oxidant genes to counteract microbead-induced oxidative stress in the
treated copepods, hence functioning in the antioxidant defense mecha­
nism; nevertheless, the microplastic-induced oxidative stress has ulti­
mately given rise to an individual response as indicated by growth
retardation and reproductive limitation in the exposed individuals
(Jeong et al., 2017). Finally, Jeong et al. (2017) proposed an adverse
outcome pathway which has linked the molecular toxic events to a
compromised individual’s fitness in the marine copepod P. nana under
8
Z. Bai et al.
exposure to PS microbeads, providing mechanistic understanding about
microplastic adverse effect in marine copepods. Similarly, in the study of
Choi et al. (2020), marine copepod T. japonicus is subjected to 50 nm and
10 μm PS beads at a concentration of 20 mg/L (50 nm: equal to
2.9 × 1011 beads/mL; 10 μm: equal to 3.6 × 104 beads/mL) for 48 h
when the ROS generation, antioxidant-related transcript levels and
antioxidant enzyme activities are measured. After exposure, micro­
plastic intake of both sizes gives rise to significant induction of ROS and
the antioxidant system is also significantly affected; taking as gluta­
thione reductase an example, both the transcript level and enzyme ac­
tivities are remarkably increased by microplastic presence (Choi et al.,
2020), together with the research (Jeong et al., 2017), implying that
oxidative stress is responsible for microplastic toxicity in marine
copepods.
Recalling that, in the real environment, marine organisms have been
confronted with stressors including microplastic contamination over
many generations, suchlike multigenerational microplastic stress study
is extremely significant. In the first multiple-generation report, micro­
plastic contamination negatively affects the important life traits (e.g.,
developmental time and fecundity) in the marine copepod T. japonicus,
but no molecular work has been performed to give mechanistic insight
into the above impact (Lee et al., 2013). In this context, ours is the first
mechanistic research that a shotgun-based quantitative proteomics is
conducted to link the microplastic-induced molecular response with its
population-level adverse outcome as exemplified by significant decrease
in survival rate and total fecundity in the copepod (T. japonicus) under
multiple-generation exposure to environmentally-realistic concentra­
tions (0.023 and 0.23 mg/L); after two generations of exposure (F0-F1),
the 0.23 mg/L microplastic treatment has strikingly enhanced several
cellular biosynthetic processes (e.g., protein synthesis and immunity
defense) and, in turn, given rise to energy depletion as a consequence of
the trade-off, ultimately compromising survival rate and total fecundity
in the stressed individuals of F1; more intriguingly, after one-generation
recovery (i.e., F2), the affected traits are completely recovered, and our
proteomics analysis demonstrates an increase of numerous critical
processes (e.g., cuticle assembly, energy metabolism, and stress-related
defense), that is, transgenerational proteome plasticity in the generation
of F2, hence giving mechanistic explanation to regaining of the
compromised physiological traits (Zhang et al., 2019). To summarize,
more multigenerational microplastic researches combining omics-based
approach and phenotypic trait analysis are urgently needed to be per­
formed in marine copepods especially under environmentally-relevant
scenarios as they should enable us to have a better mechanistic under­
standing about the biological effects of microplastics.
7. Microplastics potentially serving as vectors for toxic
chemicals in marine copepods
Regarding the high abundance, ubiquity, large surface area-to-
volume ratio and high hydrophobicity in the marine environment,
microplastics may sorb toxic pollutants (e.g., hydrophobic organic
contaminants and metals) and consequently serve as their vectors when
these toxicants are accumulated and display negative impacts in marine
organisms (Syberg et al., 2015; Wright et al., 2013). It should be
underlined that the sorption of toxic chemicals by microplastics is driven
by various interacting forces, such as van-der-Waals forces, ionic in­
teractions, and covalent bonds (Fotopoulou et al., 2014; Hartmann et al.,
2017).
Despite copepods taking a key role in marine ecosystem, only a few
works have been performed to support whether microplastics can act as
a vector for toxic compounds in this taxon (Bellas and Gil, 2020; Syberg
et al., 2017) (Table 2). For example, Syberg et al. (2017) conducted an
acute toxicity test to investigate the joint effect of PE microbeads and
triclosan (TCS) on the marine copepod Acartia tonsa; the results show
that, after 48 h exposure, the median lethal concentration (LC50) is
calculated as 157.9 μg/L for single TCS treatment, and the LC50 for
9
Ecotoxicology and Environmental Safety 217 (2021) 112243
109.6 μg/L in the combining exposure of microbeads and TCS, demon­
strating microplastics have vector effect for TCS in A. tonsa as microbead
addition strikingly potentiates its toxicity in the treated copepods.
Similarly, Bellas and Gil (2020) have also demonstrated that PE
microplastics can boost the toxicity of chlorpyrifos (CPF), a
broad-spectrum organophosphorus insecticide, in the copepod A. tonsa
because the 48-h LC50 obtained for single CPF exposure (1.34 μg/L) is
remarkably higher than for the combined treatment with microplastics
(0.37 μg/L) or CPF-loaded microplastics (0.26 μg/L), and the same trend
for the copepod’s feeding and egg production (in the case of the 48-h
median effective concentrations, 0.77 and 1.07 μg/L are calculated for
CPF, 0.03 and 0.05 μg/L for CPF combined with microplastics, and 0.18
and 0.20 μg/L for CPF-loaded microplastics, respectively). Conversely,
Beiras et al. (2019) have challenged the vector effect of microplastics to
potentiate the biological impact of hydrophobic chemicals in marine
zooplankton because they report that presence of PE microplastics
doesn’t increase the bioaccumulation of 4-n-Nonylphenol and 4-Methyl­
benzylidene-camphor and their toxicity in marine zooplankton (e.g., the
copepod A. clausi and the larva of sea urchin Paracentrotus lividus). Such
trend has also been observed in other two studies (Almeda et al., 2021;
Sørensen et al., 2020). As in the study by Sørensen et al. (2020), the
results demonstrate that presence of both microbead types (i.e., PE and
PS) insignificantly boosts the accumulation and toxicity of two poly­
cyclic aromatic hydrocarbons (i.e., fluoranthene and phenanthrene) in
marine copepods (C. finmarchicus and A. tonsa), again doubting the
vector role played by microplastics in facilitating the bioavailability of
organic compounds to marine copepods. In particular, a recent research
has investigated the combining effect of PS microplastics and dibutyl
phthalate (DBP) in the marine copepod T. japonicus under both the acute
toxicity and chronic reproduction tests; the acute testing demonstrates
that sorption to microplastcs reduces the bioavailability of DBP and
results in decreased toxicity of this chemical to the copepod; similarly,
such antagonistic interaction is also observed for the chronic repro­
duction test (Li et al., 2020). Collectively, the interactions between
microplastics and toxic compounds may be synergistic, additive, or
antagonistic in marine copepods (Almeda et al., 2021; Beiras et al.,
2019; Bellas and Gil, 2020; Li et al., 2020; Sørensen et al., 2020; Syberg
et al., 2017).
Regardless of the few researches investigating whether microplastics
can serve as vector or could increase the bioavailability of environ­
mental contaminants in marine copepods (Almeda et al., 2021; Beiras
et al., 2019; Bellas and Gil, 2020; Li et al., 2020; Sørensen et al., 2020;
Syberg et al., 2017), the above interaction may be attributed to several
aspects at least including the tested species, the type of micro­
plastics/pollutants, and their concentrations. Given the crucial niche
played by copepods in marine ecosystem and also microplastics dis­
playing huge abundance, high prevalence, persistence and large surface
area-to-volume ratio in the environment, more researches should be
performed to examine whether microplastics can act as vectors for
environmental pollutants (e.g., hydrophobic organic pollutant and
metals) in marine copepods as it should enable us to more accurately
assess the hazard risk of microplastics in marine ecosystem.
8. Implications
To summarize, the biological effects of microplastics in marine co­
pepods are ascribed to, but not restricted to, the microplastic properties
(such as age, type, shape, and size) and tested species. More importantly,
ingestion of microplastics is very common in marine copepods both
under the laboratory condition and in the environment; the consequence
is that microplastic consumption can decrease the copepod’s feeding
activity and reduce the total energy input, in the end, resulting in a
population-level adverse outcome as demonstrated by compromised
growth and reproduction in the conditioned individuals. Intriguingly,
some researches including ours have given a mechanistic understanding
concerning the negative effects of microplastics in marine copepods;
Z. Bai et al. Ecotoxicology and Environmental Safety 217 (2021) 112243

Table 3 mechanistic insights into the adverse effects of microplastics in marine

Perspectives and challenges for microplastic contamination studies.
Research topics
Multigenerational
microplastic effects
Microplastic effects coupled
with co-stressors
Molecular study
Phenotypic evaluation
Future priority issue
- More multigenerational microplastic stress
experiments should be required for numerous
marine copepods especially at environmentally
realistic concentrations in the future.
- Aged microplastics should be considered in
multiple generation studies.
- More attention should be paid to marine
copepods challenged with the combined
exposure of microplastics and co-stressors (e.g.,
food limitation, persistent organic pollutants,
and heavy metals).
- Environmentally-realistic concentration settings
for microplastics coupled with environment
contaminant are critical to assess ecological risk
for microplastic pollution.
- Omics-based studies should be done to identify
molecular biomarkers (e.g., genome,
transcriptome, and metabolome) translating
molecular toxic events to population response.
- Epigenetic approaches are needed to understand
acclimatization/adaptation mechanisms.
- Omics analysis is integrated with phenotypic
trait observation to understand molecular
mechanism at an individual level.
- Clearly interpretable measures (e.g., carrying
capacity and population genetic equilibrium)
combined with survival, fertility rates, and
suchlike important life-cycle characteristics are
needed to quantify any genetic-based phenotypic
change.
- Population genetics and phenotypic plasticity
should be integrated to obtain a robust
conclusion on the impact of microplastics on the
population dynamics of marine copepods.
copepods. It should be emphasized that physiological trait evaluation is
very important as phenotypic plasticity (i.e., the production of different
phenotypes from the same genotype) may render the copepods showing
resilience in response to stressors including microplastics. Instead, if a
stressor is too intense, then it may wipe out the most sensitive genotypes
from the copepod population, hence resulting in genetic erosion (and
consequent loss of genetic diversity), which will in turn compromise the
population’s viability in the marine environment (Ribeiro and Lopes,
2013; Venâncio et al., 2016). Correspondingly, it is urgently necessary to
investigate microplastics-driven genetic erosion in the copepods, for
example, via monitoring selectable markers (Ribeiro and Lopes, 2013)
because genetic diversity provides their potential to acclimatize/adapt
under environmental changes. To fill the above gaps, more multigen­
erational mechanistic researches (for example, via an integration of
omics-based technology, population genetics, and phenotypic trait
analysis) are required for numerous marine copepods exposed to
environmental-characteristics microplastics as demonstrated by aged
microplastics at environmentally realistic concentrations and added
with other environmental pollutants (Table 3). Collectively, suchlike
researches in marine keystone species of different trophic-levels should
not only provide mechanistic insights into the biological impacts of
microplastics, but also help make the seawater-benchmark setting and
ecological assessment for microplastics in marine environment.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgments

that is, the microplastic-induced oxidative stress and energy depletion
are mainly involved (Choi et al., 2020; Jeong et al., 2017; Zhang et al.,
2019). Particularly, our proteomics-based multigenerational exposure
research shows that transgenerational proteome plasticity may play a
key role in resilience of marine copepod in response to microplastics,
calling the urgent importance to examine the role of acclimatizatio­
n/adaptation in the response of marine copepods in against microplastic
contamination (Zhang et al., 2019). Meanwhile, despite only a few
works (Almeda et al., 2021; Beiras et al., 2019; Bellas and Gil, 2020; Li
et al., 2020; Sørensen et al., 2020; Syberg et al., 2017), microplastics can
act as vectors for environmental contaminants in marine copepods,
raising the potential that microplastics increase the bioavailability and
hazard of toxicants in marine ecosystem.
At present, much information has been provided for the biological
effects of microplastics in marine copepods, but there is still a long way
to go. Firstly, many previous researches are solely focused on the effects
of microplastics in marine copepods under short-term exposure to virgin
microbeads at far more than environmentally-realistic concentrations
(Choi et al., 2020; Heindler et al., 2017; Jeong et al., 2017; Lee et al.,
2013; Vroom et al., 2017), thereby reducing the ecological significance
of these findings. Interestingly, in contrast to virgin microplastics, the
aged ones display more adverse effects in marine organisms, which is
mainly ascribed to the latter can leach out the incorporated additives
(some of them showing endocrine disruption activity) and thus aggra­
vate the negative impacts (Fu et al., 2019; Liu et al., 2020). Secondly,
some previous works have clearly indicated that microplastics can take
as vectors of environmental contaminants (e.g., CPF and TCS) and
enhance their toxicity in marine copepods (Bellas and Gil, 2020; Syberg
et al., 2017), emphasizing the significance to find out the contribution of
microplastics (with varying ages, types, and sizes) to increased
bioavailability of environmental toxicants (especially POPs and metals)
in marine ecosystem. Finally, very scare information is available to give
This work was supported by the National Natural Science Foundation
of China (no. 41876117) and the Fundamental Research Funds for the
Central Universities (no. 20720190094).
References
Almeda, R., Rodriguez-Torres, R., Rist, S., Winding, M.H.S., Stief, P., Hansen, B.H.,
Nielsen, T.G., 2021. Microplastics do not increase bioaccumulation of petroleum
hydrocarbons in Arctic zooplankton but trigger feeding suppression under co-
exposure conditions. Sci. Total Environ. 751, 141264 https://doi.org/10.1016/j.
scitotenv.2020.141264.
Andrady, A.L., 2011. Microplastics in the marine environment. Mar. Pollut. Bull. 62,
1596–1605. https://doi.org/10.1016/j.marpolbul.2011.05.030.
Auta, H.S., Emenike, C.U., Fauziah, S.H., 2017. Distribution and importance of
microplastics in the marine environment: a review of the sources, fate, effects, and
potential solutions. Environ. Int. 102, 165–176. https://doi.org/10.1016/j.
envint.2017.02.013.
Ayukai, T., 1987. Discriminate feeding of the calanoid copepod Acartia clausi in mixtures
of phytoplankton and inert particles. Mar. Biol. 94, 579–587. https://doi.org/
10.1007/BF00431404.
Beiras, R., Muniategui-Lorenzo, S., Rodil, R., Tato, T., Montes, R., López-Ibáñez, S.,
Concha-Graña, E., Campoy-López, P., Salgueiro-González, N., Quintana, J.B., 2019.
Polyethylene microplastics do not increase bioaccumulation or toxicity of
nonylphenol and 4-MBC to marine zooplankton. Sci. Total Environ. 692, 1–9.
https://doi.org/10.1016/j.scitotenv.2019.07.106.
Bellas, J., Gil, I., 2020. Polyethylene microplastics increase the toxicity of chlorpyrifos to
the marine copepod Acartia tonsa. Environ. Pollut. 260, 114059 https://doi.org/
10.1016/j.envpol.2020.114059.
Boerger, C.M., Lattin, G.L., Moore, S.L., Moore, C.J., 2010. Plastic ingestion by
planktivorous fishes in the North Pacific Central Gyre. Mar. Pollut. Bull. 60,
2275–2278. https://doi.org/10.1016/j.marpolbul.2010.08.007.
Botterell, Z.L., Beaumont, N., Cole, M., Hopkins, F.E., Steinke, M., Thompson, R.C.,
Lindeque, P.K., 2020. Bioavailability of microplastics to marine zooplankton: effect
of shape and infochemicals. Environ. Sci. Technol. 54, 12024–12033. https://doi.
org/10.1021/acs.est.0c02715.
Botterell, Z.L.R., Beaumont, N., Dorrington, T., Steinke, M., Thompson, R.C., Lindeque, P.
K., 2019. Bioavailability and effects of microplastics on marine zooplankton: a
review. Environ. Pollut. 245, 98–110. https://doi.org/10.1016/j.
envpol.2018.10.065.
Browne, M.A., Dissanayake, A., Galloway, T.S., Lowe, D.M., Thompson, R.C., 2008.
Ingested microscopic plastic translocates to the circulatory system of the mussel,

10
Z. Bai et al.
Mytilus edulis (L.). Environ. Sci. Technol. 42, 5026–5031. https://doi.org/10.1021/
es800249a.
Cheng, Y., Wang, J., Yi, X., Li, L., Liu, X., Ru, S., 2020. Low microalgae availability
increases the ingestion rates and potential effects of microplastics on marine
copepod Pseudodiaptomus annandalei. Mar. Pollut. Bull. 152, 110919 https://doi.
org/10.1016/j.marpolbul.2020.110919.
Choi, J.S., Hong, S.H., Park, J.-W., 2020. Evaluation of microplastic toxicity in
accordance with different sizes and exposure times in the marine copepod Tigriopus
japonicus. Mar. Environ. Res. 153, 104838 https://doi.org/10.1016/j.
marenvres.2019.104838.
Choi, J.S., Jung, Y.-J., Hong, N.-H., Hong, S.H., Park, J.-W., 2018. Toxicological effects of
irregularly shaped and spherical microplastics in a marine teleost, the sheepshead
minnow (Cyprinodon variegatus). Mar. Pollut. Bull. 129, 231–240. https://doi.org/
10.1016/j.marpolbul.2018.02.039.
Clark, J.R., Cole, M., Lindeque, P.K., Fileman, E., Blackford, J., Lewis, C., Lenton, T.M.,
Galloway, T.S., 2016. Marine microplastic debris: a targeted plan for understanding
and quantifying interactions with marine life. Front. Ecol. Environ. 14, 317–324.
https://doi.org/10.1002/fee.1297.
Cole, M., Coppock, R., Lindeque, P.K., Altin, D., Reed, S., Pond, D.W., Sørensen, L.,
Galloway, T.S., Booth, A.M., 2019. Effects of nylon microplastic on feeding, lipid
accumulation, and moulting in a coldwater copepod. Environ. Sci. Technol. 53,
7075–7082. https://doi.org/10.1021/acs.est.9b01853.
Cole, M., Lindeque, P.K., Fileman, E., Clark, J., Lewis, C., Halsband, C., Galloway, T.S.,
2016. Microplastics alter the properties and sinking rates of zooplankton faecal
pellets. Environ. Sci. Technol. 50, 3239–3246. https://doi.org/10.1021/acs.
est.5b05905.
Cole, M., Lindeque, P., Fileman, E., Halsband, C., Galloway, T.S., 2015. The impact of
polystyrene microplastics on feeding, function and fecundity in the marine copepod
Calanus helgolandicus. Environ. Sci. Technol. 49, 1130–1137. https://doi.org/
10.1021/es504525u.
Cole, M., Lindeque, P., Fileman, E., Halsband, C., Goodhead, R., Moger, J., Galloway, T.
S., 2013. Microplastic ingestion by zooplankton. Environ. Sci. Technol. 47,
6646–6655. https://doi.org/10.1021/es400663f.
Coppock, R.L., Galloway, T.S., Cole, M., Fileman, E.S., Queirós, A.M., Lindeque, P.K.,
2019. Microplastics alter feeding selectivity and faecal density in the copepod,
Calanus helgolandicus. Sci. Total Environ. 687, 780–789. https://doi.org/10.1016/j.
scitotenv.2019.06.009.
Costa, E., Piazza, V., Lavorano, S., Faimali, M., Garaventa, F., Gambardella, C., 2020.
Trophic transfer of microplastics from copepods to jellyfish in the marine
environment. Front. Environ. Sci. 8, 158. https://doi.org/10.3389/
fenvs.2020.571732.
Cózar, A., Echevarría, F., González-Gordillo, J.I., Irigoien, X., Úbeda, B., Hernández-
León, S., Palma, Á.T., Navarro, S., García-de-Lomas, J., Ruiz, A., Fernández-de-
Puelles, M.L., Duarte, C.M., 2014. Plastic debris in the open ocean. Proc. Natl. Acad.
Sci. 111, 10239–10244. https://doi.org/10.1073/pnas.1314705111.
La Daana, K.K., Officer, R., Lyashevska, O., Thompson, R.C., O’Connor, I., 2017.
Microplastic abundance, distribution and composition along a latitudinal gradient in
the Atlantic Ocean. Mar. Pollut. Bull. 115, 307–314. https://doi.org/10.1016/j.
marpolbul.2016.12.025.
Desforges, J.-P.W., Galbraith, M., Ross, P.S., 2015. Ingestion of microplastics by
zooplankton in the Northeast Pacific Ocean. Arch. Environ. Contam. Toxicol. 69,
320–330. https://doi.org/10.1007/s00244-015-0172-5.
Engler, R.E., 2012. The complex interaction between marine debris and toxic chemicals
in the ocean. Environ. Sci. Technol. 46, 12302–12315. https://doi.org/10.1021/
es3027105.
Eriksen, M., Lebreton, L.C.M., Carson, H.S., Thiel, M., Moore, C.J., Borerro, J.C.,
Galgani, F., Ryan, P.G., Reisser, J., 2014. Plastic pollution in the world’s oceans:
more than 5 trillion plastic pieces weighing over 250,000 tons afloat at sea. PLoS
One 9, e111913. https://doi.org/10.1371/journal.pone.0111913.
Espinosa, C., Esteban, M.Á., Cuesta, A., 2019. Dietary administration of PVC and PE
microplastics produces histological damage, oxidative stress and immunoregulation
in European sea bass (Dicentrarchus labrax L.). Fish. Shellfish Immun. 95, 574–583.
https://doi.org/10.1016/j.fsi.2019.10.072.
Fotopoulou, K.N., Vakros, J., Karapanagioti, H.K., 2014, Surface properties of marine
microplastics that affect their interaction with pollutants and microbes. In CIESM
Workshop Monographs 46, pp. 377–381.
Fueser, H., Mueller, M.T., Traunspurger, W., 2020. Ingestion of microplastics by
meiobenthic communities in small-scale microcosm experiments. Sci. Total Environ.
746, 141276 https://doi.org/10.1016/j.scitotenv.2020.141276.
Fu, D., Zhang, Q., Fan, Z., Qi, H., Wang, Z., Peng, L., 2019. Aged microplastics polyvinyl
chloride interact with copper and cause oxidative stress towards microalgae Chlorella
vulgaris. Aquat. Toxicol. 216, 105319 https://doi.org/10.1016/j.
aquatox.2019.105319.
Gunaalan, K., Fabbri, E., Capolupo, M., 2020. The hidden threat of plastic leachates: a
critical review on their impacts on aquatic organisms. Water Res. 184, 116170
https://doi.org/10.1016/j.watres.2020.116170.
Harrison, J.P., Sapp, M., Schratzberger, M., Osborn, A.M., 2011. Interactions between
microorganisms and marine microplastics: a call for research. Mar. Technol. Soc. J.
45, 12–20. https://doi.org/10.4031/MTSJ.45.2.2.
Hartmann, N.B., Rist, S., Bodin, J., Jensen, L.H., Schmidt, S.N., Mayer, P., Meibom, A.,
Baun, A., 2017. Microplastics as vectors for environmental contaminants: exploring
sorption, desorption, and transfer to biota. Integr. Environ. Assess. 13, 488–493.
https://doi.org/10.1002/ieam.1904.
Heindler, F.M., Alajmi, F., Huerlimann, R., Zeng, C., Newman, S.J., Vamvounis, G., van
Herwerden, L., 2017. Toxic effects of polyethylene terephthalate microparticles and
Di(2-ethylhexyl)phthalate on the calanoid copepod, Parvocalanus crassirostris.
11
Ecotoxicology and Environmental Safety 217 (2021) 112243
Ecotoxicol. Environ. Saf. 141, 298–305. https://doi.org/10.1016/j.
ecoenv.2017.03.029.
Hidalgo-Ruz, V., Gutow, L., Thompson, R.C., Thiel, M., 2012. Microplastics in the marine
environment: a review of the methods used for identification and quantification.
Environ. Sci. Technol. 46, 3060–3075. https://doi.org/10.1021/es2031505.
Jahnke, A., Arp, H.P.H., Escher, B.I., Gewert, B., Gorokhova, E., Kühnel, D.,
Ogonowski, M., Potthoff, A., Rummel, C., Schmitt-Jansen, M., Toorman, E.,
MacLeod, M., 2017. Reducing uncertainty and confronting ignorance about the
possible impacts of weathering plastic in the marine environment. Environ. Sci.
Tech. Let. 4, 85–90. https://doi.org/10.1021/acs.estlett.7b00008.
Jambeck, J.R., Geyer, R., Wilcox, C., Siegler, T.R., Perryman, M., Andrady, A.,
Narayan, R., Law, K.L., 2015. Plastic waste inputs from land into the ocean. Science
347, 768–771. https://doi.org/10.1126/science.1260352.
Jeong, C.-B., Kang, H.-M., Lee, M.-C., Kim, D.-H., Han, J., Hwang, D.-S., Souissi, S.,
Lee, S.-J., Shin, K.-H., Park, H.G., Lee, J.-S., 2017. Adverse effects of microplastics
and oxidative stress-induced MAPK/Nrf2 pathway-mediated defense mechanisms in
the marine copepod Paracyclopina nana. Sci. Rep. 7, 41323. https://doi.org/
10.1038/srep41323.
Kooi, M., Nes, E.Hv, Scheffer, M., Koelmans, A.A., 2017. Ups and downs in the ocean:
effects of biofouling on vertical transport of microplastics. Environ. Sci. Technol. 51,
7963–7971. https://doi.org/10.1021/acs.est.6b04702.
Law, K.L., 2017. Plastics in the marine environment. Annu. Rev. Mar. Sci. 9, 205–229.
https://doi.org/10.1146/annurev-marine-010816-060409.
Lee, K.-W., Shim, W.J., Kwon, O.Y., Kang, J.-H., 2013. Size-dependent effects of micro
polystyrene particles in the marine copepod Tigriopus japonicus. Environ. Sci.
Technol. 47, 11278–11283. https://doi.org/10.1021/es401932b.
Lindeque, P.K., Cole, M., Coppock, R.L., Lewis, C.N., Miller, R.Z., Watts, A.J.,
Galloway, T.S., 2020. Are we underestimating microplastic abundance in the marine
environment? A comparison of microplastic capture with nets of different mesh-size.
Environ. Pollut. 265, 114721 https://doi.org/10.1016/j.envpol.2020.114721.
Liu, P., Wu, X., Liu, H., Wang, H., Lu, K., Gao, S., 2020. Desorption of pharmaceuticals
from pristine and aged polystyrene microplastics under simulated gastrointestinal
conditions. J. Hazard. Mater. 392, 122346 https://doi.org/10.1016/j.
jhazmat.2020.122346.
Li, Z., Zhou, H., Liu, Y., Zhan, J., Li, W., Yang, K., Yi, X., 2020. Acute and chronic
combined effect of polystyrene microplastics and dibutyl phthalate on the marine
copepod Tigriopus japonicus. Chemosphere 261, 127711. https://doi.org/10.1016/j.
chemosphere.2020.127711.
Lobelle, D., Cunliffe, M., 2011. Early microbial biofilm formation on marine plastic
debris. Mar. Pollut. Bull. 62, 197–200. https://doi.org/10.1016/j.
marpolbul.2010.10.013.
Lusher, A.L., McHugh, M., Thompson, R.C., 2013. Occurrence of microplastics in the
gastrointestinal tract of pelagic and demersal fish from the English Channel. Mar.
Pollut. Bull. 67, 94–99. https://doi.org/10.1016/j.marpolbul.2012.11.028.
Ma, H., Pu, S., Liu, S., Bai, Y., Mandal, S., Xing, B., 2020. Microplastics in aquatic
environments: toxicity to trigger ecological consequences. Environ. Pollut. 261,
114089 https://doi.org/10.1016/j.envpol.2020.114089.
Mei, W., Chen, G., Bao, J., Song, M., Li, Y., Luo, C., 2020. Interactions between
microplastics and organic compounds in aquatic environments: a mini review. Sci.
Total Environ. 736, 139472 https://doi.org/10.1016/j.scitotenv.2020.139472.
Murray, F., Cowie, P.R., 2011. Plastic contamination in the decapod crustacean Nephrops
norvegicus (Linnaeus, 1758). Mar. Pollut. Bull. 62, 1207–1217. https://doi.org/
10.1016/j.marpolbul.2011.03.032.
Naqash, N., Prakash, S., Kapoor, D., Singh, R., 2020. Interaction of freshwater
microplastics with biota and heavy metals: a review. Environ. Chem. Lett. 245, 1–12.
https://doi.org/10.1007/s10311-020-01044-3.
Oberbeckmann, S., Löder, M.G.J., Labrenz, M., 2015. Marine microplastic-associated
biofilms − a review. Environ. Chem. 12, 551–562. https://doi.org/10.1071/
EN15069.
Onink, V., Wichmann, D., Delandmeter, P., van Sebille, E., 2019. The role of Ekman
currents, geostrophy, and stokes drift in the accumulation of floating microplastic.
J. Geophys. Res.-Oceans 124, 1474–1490. https://doi.org/10.1029/2018JC014547.
Outram, L., Hurley, J., Rott, A., Crooks, N., Pernetta, A.P., 2020. No evidence of
microplastic consumption by the copepod, Temora longicornis (Müller, 1785) in
Chichester Harbour, United Kingdom. Nauplius 28. https://doi.org/10.1590/2358-
2936e2020033.
Ribeiro, R., Lopes, I., 2013. Contaminant driven genetic erosion and associated
hypotheses on alleles loss, reduced population growth rate and increased
susceptibility to future stressors: an essay. Ecotoxicology 22, 889–899. https://doi.
org/10.1007/s10646-013-1070-0.
Rodrigues, J.P., Duarte, A.C., Santos-Echeandía, J., Rocha-Santos, T., 2019. Significance
of interactions between microplastics and POPs in the marine environment: a critical
overview. TrAC-Trends Anal. Chem. 111, 252–260. https://doi.org/10.1016/j.
trac.2018.11.038.
Rodríguez-Torres, R., Almeda, R., Kristiansen, M., Rist, S., Winding, M.S., Nielsen, T.G.,
2020. Ingestion and impact of microplastics on arctic Calanus copepods. Aquat.
Toxicol. 228, 105631 https://doi.org/10.1016/j.aquatox.2020.105631.
Van Sebille, E., Wilcox, C., Lebreton, L., Maximenko, N., Hardesty, B.D., Van Franeker, J.
A., Eriksen, M., Siegel, D., Galgani, F., Law, K.L., 2015. A global inventory of small
floating plastic debris. Environ. Res. Lett. 10, 124006 https://doi.org/10.1088/
1748-9326/10/12/124006.
Setälä, O., Fleming-Lehtinen, V., Lehtiniemi, M., 2014. Ingestion and transfer of
microplastics in the planktonic food web. Environ. Pollut. 185, 77–83. https://doi.
org/10.1016/j.envpol.2013.10.013.
Sun, X., Liu, T., Zhu, M., Liang, J., Zhao, Y., Zhang, B., 2018. Retention and
characteristics of microplastics in natural zooplankton taxa from the East China Sea.
Z. Bai et al.
Sci. Total Environ. 640–641, 232–242. https://doi.org/10.1016/j.
scitotenv.2018.05.308.
Sun, X., Li, Q., Zhu, M., Liang, J., Zheng, S., Zhao, Y., 2017. Ingestion of microplastics by
natural zooplankton groups in the northern South China Sea. Mar. Pollut. Bull. 115,
217–224. https://doi.org/10.1016/j.marpolbul.2016.12.004.
Sussarellu, R., Suquet, M., Thomas, Y., Lambert, C., Fabioux, C., Pernet, M.E.J., Le
Goïc, N., Quillien, V., Mingant, C., Epelboin, Y., Corporeau, C., Guyomarch, J.,
Robbens, J., Paul-Pont, I., Soudant, P., Huvet, A., 2016. Oyster reproduction is
affected by exposure to polystyrene microplastics. Proc. Natl. Acad. Sci. U. S. A. 113,
2430–2435. https://doi.org/10.1073/pnas.1519019113.
Suwaki, C.H., De-La-Cruz, L.T., Lopes, R.M., 2020. Impacts of microplastics on the
swimming behavior of the copepod Temora turbinata (Dana, 1849). Fluids 5, 103.
https://doi.org/10.3390/fluids5030103.
Syberg, K., Khan, F.R., Selck, H., Palmqvist, A., Banta, G.T., Daley, J., Sano, L.,
Duhaime, M.B., 2015. Microplastics: addressing ecological risk through lessons
learned. Environ. Toxicol. Chem. 34, 945–953. https://doi.org/10.1002/etc.2914.
Syberg, K., Nielsen, A., Khan, F.R., Banta, G.T., Palmqvist, A., Jepsen, P.M., 2017.
Microplastic potentiates triclosan toxicity to the marine copepod Acartia tonsa
(Dana). J. Toxicol. Environ. Heal. A 80, 1369–1371. https://doi.org/10.1080/
15287394.2017.1385046.
Sørensen, L., Rogers, E., Altin, D., Salaberria, I., Booth, A.M., 2020. Sorption of PAHs to
microplastic and their bioavailability and toxicity to marine copepods under co-
exposure conditions. Environ. Pollut. 258, 113844 https://doi.org/10.1016/j.
envpol.2019.113844.
Turner, J.T., 2015. Zooplankton fecal pellets, marine snow, phytodetritus and the
ocean’s biological pump. Prog. Oceanogr. 130, 205–248. https://doi.org/10.1016/j.
pocean.2014.08.005.
Venâncio, C., Ribeiro, R., Soares, A.M., Lopes, I., 2016. Multiple stressor differential
tolerances: possible implications at the population level. PLoS One 11, e0151847.
https://doi.org/10.1371/journal.pone.0151847.
12
Ecotoxicology and Environmental Safety 217 (2021) 112243
Vroom, R.J.E., Koelmans, A.A., Besseling, E., Halsband, C., 2017. Aging of microplastics
promotes their ingestion by marine zooplankton. Environ. Pollut. 231, 987–996.
https://doi.org/10.1016/j.envpol.2017.08.088.
Wang, S., Chen, H., Zhou, X., Tian, Y., Lin, C., Wang, W., Lin, H., 2020. Microplastic
abundance, distribution and composition in the mid-west Pacific Ocean. Environ.
Pollut. 264, 114125 https://doi.org/10.1016/j.envpol.2020.114125.
Welden, N.A.C., Cowie, P.R., 2016. Environment and gut morphology influence
microplastic retention in langoustine, Nephrops norvegicus. Environ. Pollut. 214,
859–865. https://doi.org/10.1016/j.envpol.2016.03.067.
Wesch, C., Bredimus, K., Paulus, M., Klein, R., 2016. Towards the suitable monitoring of
ingestion of microplastics by marine biota: a review. Environ. Pollut. 218,
1200–1208. https://doi.org/10.1016/j.envpol.2016.08.076.
Wilson, D.S., 1973. Food size selection among copepods. Ecology 54, 909–914. https://
doi.org/10.2307/1935688.
Wright, S.L., Thompson, R.C., Galloway, T.S., 2013. The physical impacts of
microplastics on marine organisms: a review. Environ. Pollut. 178, 483–492. https://
doi.org/10.1016/j.envpol.2013.02.031.
Yu, J., Tian, J.Y., Xu, R., Zhang, Z.Y., Yang, G.P., Wang, X.D., Chen, R., 2020. Effects of
microplastics exposure on ingestion, fecundity, development, and dimethylsulfide
production in Tigriopus japonicus (Harpacticoida, copepod). Environ. Pollut. 267,
115429 https://doi.org/10.1016/j.envpol.2020.115429.
Zettler, E.R., Mincer, T.J., Amaral-Zettler, L.A., 2013. Life in the “plastisphere”:
microbial communities on plastic marine debris. Environ. Sci. Technol. 47,
7137–7146. https://doi.org/10.1021/es401288x.
Zhang, C., Jeong, C.-B., Lee, J.-S., Wang, D., Wang, M., 2019. Transgenerational
proteome plasticity in resilience of a marine copepod in response to environmentally
relevant concentrations of microplastics. Environ. Sci. Technol. 53, 8426–8436.
https://doi.org/10.1021/acs.est.9b02525.
Zhang, W., Zhang, S., Zhao, Q., Qu, L., Ma, D., Wang, J., 2020. Spatio-temporal
distribution of plastic and microplastic debris in the surface water of the Bohai Sea.
Mar. Pollut. Bull. 158, 111343 https://doi.org/10.1016/j.marpolbul.2020.111343.