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Review

Progress on the Effects of Microplastics on Aquatic Crustaceans: A Review

by
Siyi Zhang
,
Haodi Wu
and
Jing Hou
*
MOE Key Laboratory of Resources and Environmental Systems Optimization, College of Environmental Science and Engineering, North China Electric Power University, Beijing 102206, China
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2023, 24(6), 5523; https://doi.org/10.3390/ijms24065523
Submission received: 9 February 2023 / Revised: 5 March 2023 / Accepted: 11 March 2023 / Published: 14 March 2023
(This article belongs to the Section Materials Science)
Browse Figures
Versions Notes

Abstract

:
It is impossible to overlook the effects of microplastics on aquatic life as they continuously accumulate in aquatic environments. Aquatic crustaceans, as both predator and prey, play an important role in the food web and energy transmission. It is of great practical significance to pay attention to the toxic effects of microplastics on aquatic crustaceans. This review finds that most studies have shown that microplastics negatively affect the life history, behaviors and physiological functions of aquatic crustaceans under experimental conditions. The effects of microplastics of different sizes, shapes or types on aquatic crustaceans are different. Generally, smaller microplastics have more negative effects on aquatic crustaceans. Irregular microplastics have more negative effects on aquatic crustaceans than regular microplastics. When microplastics co-exist with other contaminants, they have a greater negative impact on aquatic crustaceans than single contaminants. This review contributes to rapidly understanding the effects of microplastics on aquatic crustaceans, providing a basic framework for the ecological threat of microplastics to aquatic crustaceans.

1. Introduction

With the increase in plastic production, use and emissions, 275 million metric tons of plastic waste were generated in 192 coastal countries, of which 4.8–12.7 million metric tons entered the sea in 2010 [1]. As of 2015, approximately 6300 million metric tons of plastic waste had been generated, and by 2050, nearly 12,000 million metric tons of plastic waste is expected to enter landfills or the natural environment [2]. Plastics could form microplastics through mechanical [3], photochemical [4] and biological [5] processes. Microplastics were first proposed in 2004 [6] and were considered as plastic debris <5 mm, whilst plastic debris <100 nm were considered nanoplastics [7]. Currently, microplastics have been detected in the oceans [8,9,10], freshwater [11], underground water [12], rivers [13], polar regions [14] and even in drinking water [15]. Microplastics have also been detected in aquatic organisms such as seabirds [16], turtles [17], zooplankton [18], fishes [19], mammals [20], crustaceans [21] and bivalves [22]. Studies have found that microplastics have negative effects on aquatic organisms, such as changes in feeding ability [23] and swimming behavior [24], malformation [25], oxidative stress response [26], growth and development toxicity [27], reproductive toxicity [28], neurotoxicity [29], immunotoxicity [30], etc.
As a ubiquitous aquatic organism in freshwater and marine environments, aquatic crustaceans are widely used in experimental studies due to their wide distribution, rapid reproduction and toxicity sensitivity. Aquatic crustaceans play an important role in the food web and energy transmission. They can be predators to plants, algae and other smaller creatures, as well as food sources for other prey. Aquatic crustaceans such as Neomysis integer [31] and Gammarus duebeni [32] could act as predators, while other aquatic crustaceans such as Tigriopus fulvus [33], Daphnia magna [34,35] and Neomysis spp. [36] could serve as food for other creatures. Aquatic crustaceans could also act as carriers of microplastics in the food chain. For example, in the food chain of Raphidocelis subcapitata–D. magna–Pimephales promelas, D. magna act as both predator and prey, and microplastics were found to be transferred to the highest nutritional level of the food chain [34]. The aquatic crustaceans commonly used in experimental studies are Cladocera, Decapoda, Copepoda, Anostraca, Amphipoda, Cirripedia, Isopoda, etc. The Cladocera are key zooplankton species in aquatic ecosystems that could be eaten by any freshwater predator [37], among which the most typical, D. magna, has the advantages of a large size, short life cycle, high fecundity and parthenogenesis [38]. Decapoda represent a diverse taxon within the aquatic crustaceans, which are rich in species and play an important role in ecology and the economy [39], and some Decapoda are globally important seafood products with high value in commercial fisheries and aquaculture [40]. Copepoda, the second largest crustacean taxa, are widely distributed and play an important role in the transport of contaminants across the food chain [41]. Anostraca are unquestionably the most taxonomically diverse group at all levels [42]. Amphipoda are widely distributed in marine and freshwater environments and represent the dominant macroinvertebrates in biomass in many river communities [43]. Cirripedia are one of the most common marine crustaceans [44]. Additionally, Isopoda could survive in a variety of water environments and are one of the most abundant groups in marine ecosystems [45].
To date, experimental studies on the effects of microplastics on aquatic organisms have mainly focused on shellfish and fish, whilst aquatic crustaceans have not been comprehensively reviewed. Therefore, we specifically reviewed the effects of microplastics on aquatic crustaceans in terms of life history, behaviors, physiological functions and molecular response mechanisms (Figure 1). The keywords “microplastics”, “crustacean”, “Cladocera (cladoceran)”, “Decapoda (decapod)”, “Copepoda (copepod)”, “Anostraca”, “Amphipoda (amphipod)”, “Cirripedia (barnacle)” and “Isopoda (isopod)” were retrieved jointly in the database. The aquatic crustaceans were classified by referring to the classification of the National Center for Biotechnology Information (NCBI). This review only summarized experimental studies with independent experiments, and did not review other external factors such as pH, temperature, etc. A total of 239 papers meeting the above criteria were retrieved. Among them, there were 200 papers (83.68%) on life history (Table S1), 61 papers (25.52%) on behaviors (Table S2), 79 papers (33.05%) on physiological functions (Table S3) and 57 papers (23.85%) on molecular response mechanisms (Table S4). This review contributes to rapidly understanding the effects of microplastics on aquatic crustaceans, providing a basic framework for the ecological threat of microplastics to aquatic crustaceans.

2. Effects of Microplastics on Life History of Aquatic Crustaceans

Two hundred papers dealing with the study of the effects of microplastics on the life history of aquatic crustaceans were found, including survival (167 papers, 83.50%), growth and development (99 papers, 49.50%) and reproduction (81 papers, 40.50%) (Figure 2A). Among these, 111 papers focused on Cladocera (8 species), 29 papers on Decapoda (17 species), 25 papers on Copepoda (16 species), 19 papers on Anostraca (3 species), 15 papers on Amphipoda (9 species), 7 papers on Cirripedia (10 species) and 3 papers on Isopoda (2 species) (Figure 2B). The most studied Cladocera were D. magna and Daphnia pulex. The most studied Decapoda were Litopenaeus vannamei and Macrobrachium nipponense. The most studied Copepoda were Tigriopus japonicus and Acartia tonsa. The Artemia franciscana and Amphibalanus amphitrite were the most studied Anostraca and Cirripedia, respectively. The most extensively utilized types of microplastics were polystyrene (PS) (118 papers, 59.00%), polyethylene (PE) (44 papers, 22.00%), polypropylene (PP) (13 papers, 6.50%), polyethylene terephthalate (PET) (13 papers, 6.50%) and polyvinyl chloride (PVC) (8 papers, 4.00%), whilst the most extensively utilized shapes were microspheres (76 papers, 38.00%), microbeads (41 papers, 20.50%), microfibers (21 papers, 10.50%) and fragments (14 papers, 7.00%).

2.1. Survival

For Cladocera, D. magna was the most concerned species. It has been found that 52 nm [35] and 100–120 nm amino-PS (PS- NH 2 ) [46,47] reduced D. magna survival in a dose-dependent manner within the range of 1–400 mg/L. However, 0–1.5 μm PS significantly increased D. magna immobilization followed by 10–60 and 60–230 μm PS [48]. The 48-h median effect concentrations ( EC 50 ) of amidine PS and carboxyl PS were 36.2 ± 4.1 mg/L and 111.4 ± 15.2 mg/L [49], the 24 h EC 50 of PS- NH 2 and carboxylated-PS (PS-COOH) was 25.8 mg/L and 36.3 mg/L [23], whilst the 48 h median lethal concentrations ( LC 50 ) of plain PS, negative PS- NH 2 and PS-COOH was 5.24, 8.56 and 20.2 mg/L to D. magna [50], respectively. Pristine PS could significantly decrease D. magna survival, while aged PS caused no significant effects [51]. PS and deltamethrin (DM) produced synergistic effects on D. magna survival [52]. The same went for PS and glyphosate (Gly) [53]. On the contrary, humic substances reduced the PS- NH 2 toxicity to D. magna survival based on their composition and corona formation [46]. Similarly, humic acid could alleviate the toxicity of PS- NH 2 [47]. Additionally, the combined effects of PS combined with the heavy metals lead (Pb), copper (Cu), cadmium (Cd) and nickel (Ni) on D. magna survival changed from antagonistic to additive as the concentration of PS increased [54]. The 48 h EC 50 of 37.24 ± 11.76 μm PE fragments and 37.05 ± 3.96 μm PE beads to D. magna was 3.9 mg/L and 323 mg/L, respectively [55]. The survival rate of D. magna caused by 17.23 ± 3.43 µm PE fragments, 34.43 ± 13.09 µm fragments and 40–48 µm beads was 20%, 60% and 90%, respectively [56]. Pristine PE showed more negative effects on D. magna survival than biofouled PE, and found that the LC 50 of pristine PE to D. magna dropped from 485 to 1.26 mg/L during a period of 72 h to 7 days [57]. It was found that 37.24 ± 11.76 μm PE fragments and benzophenone-3 (BP-3) had synergistic effects on reducing the D. magna survival, the 48 h EC 50 of PE and mixture of PE and BP-3 was 3.9 and 0.99 mg/L [55]. For other Cladocera species, 48 h LC 50 of 75 nm PS to D. pulex was 76.69 mg/L [58]. The forty-eight-hour LC50 of PE beads and polyester fibers to Ceriodaphnia dubia was 2.2 mg/L and 1.5 mg/L, respectively [24]. Primary microplastics reduced the C. dubia survival more than secondary microplastics [59].
For Decapoda, 75 nm PS significantly reduced M. nipponense survival in a dose-dependent manner within the range of 5–40 mg/L [60]. It was also found that 1 and 10 μm PS reduced Neomysis awatschensis survival in a dose-dependent manner within the range of 1 × 10 3 –5 × 10 5 particles/mL [61]. The 96-h LC 50 of 75 nm PS to M. nipponense was 396.391 mg/L [62]. PS–COOH reduced Neomysis japonic survival more than PS within the range of 10–1250 μg/L [63]. PE reduced the survival of shrimps (Penaeus monodon, Marsupenaeus japonicas, L. vannamei) in dose-dependent manner within the range of 25–300 mg/L [64]. PE significantly reduced L. vannamei survival at 5000 μg/L [65] or at 0.5 and 1 μg/g shrimp [66]. The 93 μm fibers reduced Palaemonetes pugio survival more than fragment and spheres [67]. High-density polyethylene (HDPE) and malathion (MLT) had synergistic effects on decreasing Minuca ecuadoriensis survival [68].
For Copepoda, 0.05 μm PS caused the highest negative effects on T. japonicus survival followed by 0.5 μm PS and 6 μm PS had no effects within the range of 0.125–25 mg/L [69]. Chlorpyrifos (CPF) increased the effects caused by HDPE on reducing A. tonsa survival [70]. PE and triclosan (TCS) produced synergistic effects on reducing A. tonsa survival [71]. For Anostraca, the 48 h LC 50 of 50–70 nm PS and 100–120 nm PS to Artemia salina was 4.82 mg/L and 8.79 mg/L, respectively [72]. Plain PS, PS-COOH and PS- NH 2 co-existed with nano- TiO 2 altered A. salina survival [73]. For Amphipoda, PE significantly reduced Hyalella azteca survival at 1000 and 10,000 plastics/mL [74]. Tire wear particles reduced H. azteca survival in a dose-dependent within the range of 0–15,000 particles/mL [75]. For Anostraca, the 24-h EC 50 of amidine PS and carboxyl PS to Thamnocephalus platyurus was 194.8 ± 17.6 mg/L and 318.2 ± 66.9 mg/L, respectively [49]. Additionally, for Cirripedia, PVC significantly reduced A. amphitrite survival compared to PS and polymethyl methacrylate (PMMA) at 15 and 25 mg/L [76].

2.2. Growth and Development

For Cladocera, D. magna was the most concerned species. PS significantly reduced the D. magna body size at 2000 particles/mL [77,78] and within the range of 5–100 mg/L [79]. Six-micrometer PS spheres significantly reduced the D. magna body length at 500 particles/mL [80]. Ten-micrometer PS affected D. magna body length at 0.125, 1.25 and 12.5 mg/L, while one-micrometer PS had no significant effect [81]. PS significantly reduced D. magna growth at 1 and 2 mg/L, and PS co-existed with TCS or methyl-triclosan (MTCS) caused more growth reduction than that which co-existed with triclocarban (TCC) [82]. PE reduced the D. magna growth-like body size, lifespan, etc., in a dose-dependent manner at 5, 20 and 40 mg/L [83]. PE fragments of 17.23 ± 3.43 µm significantly decreased the D. magna body length, while 34.43 ± 13.09 µm fragments and 40–48 µm beads caused no effects [56]. PE co-existed with DM resulted higher negative effects on D. magna growth than single PE [52]. For other Cladocera species, 75 nm PS affected D. pulex growth within the range of 0.1–2 mg/L [58]. Moreover, 0.7 µm PS caused more negative effects on growth of D. pulex and Moina macrocopa than 1 µm PS [84]. PE beads and polyester fibers significantly reduced the C. dubia body size at 2000 μg/L, and 500 and 1000 μg/L, respectively [24]. PE co-existed with Cd reduced Moina monogolica growth more significantly than single PE around 16% and 10% when PE was 300 μg/L [85]. On the contrary, PE and Cu had an antagonistic interaction on Daphnia carinata molting frequency [86].
For Decapoda, 75 nm PS affected the M. nipponense growth within the range of 5–40 mg/L [60]. PS and PS-COOH induced Neomysis japonica growth inhibition within the range of 250–6250 μg/L, and PS-COOH had significantly greater growth inhibition [63]. Both PS and PE reduced the length and weight of Macrobrachium rosenbergii in a dose-dependent manner at 1, 5 and 10 mg/100 g in food [87]. PP fibers significantly affected the growth of Carcinus maenas at 0.3%, 0.6% and 1% in food [88]. For Copepoda, 0.05 μm PS significantly reduced the Paracyclopina nana growth rate at 10 and 20 mg/L, while 0.5 and 6 μm PS had no significant effect [89]. Whilst the 0.05 μm PS significantly delayed the development time of T. japonicus in F0 and F1 generations at 1.25 mg/L, the 0.5 μm PS significantly delayed development in F1 generation at 25 mg/L and the 6 μm ones caused no effects [69]. Additionally, 6.58 µm PS significantly delayed the development time of Nitokra lacustris pacifca at 700 beads/mL [90]. For Anostraca, PS- NH 2 significantly reduced body length of A. franciscana at 1 and 10 mg/L [91]. PS and PE significantly reduced the Artemia parthenogenetica growth rate and body length at 100 mg/L, and PE had a higher inhibition effect on the growth rate [92]. Additionally, for Amphipoda, PS significantly inhibited the Gammarus pulex growth in a dose-dependent manner within the range of 10–40% PS weight in sediment, but had no effect on H. azteca [93]. However, PE particles (5000 and 10,000 particles/mL) and PP fibers (45 and 90 fibers/mL) significantly reduced the dry weight of H. azteca [74]. Tire wear particles significantly decreased the growth of H. azteca at 1000 and 2000 particles/mL [75].

2.3. Reproduction

For Cladocera D. magna, 200 nm PS decreased the number of broods produced by D. magna compared to 600 nm PS [94]. Pristine PS and aged PS significantly inhibited the D. magna reproduction at the 10 5 particles/mL concentration level [51]. Moreover, 10,000 particles/mL pristine PS led to the extinction of D. magna in F2 generation [78], and 2000 and 10,000 particles/mL secondary PS led to extinction in F3 and F0 generations [77], respectively. Interestingly, 1 and 10 μm PS unexpectedly significantly increased D. magna reproduction at 12.5 mg/L [81]. The co-existence of PS and other contaminants could cause synergistic toxicity on D. magna reproduction, such as PS and DM [52], PS and Gly [53], PS and benzo(a)pyrene (BaP) [94] and PS-COOH and zinc (Zn) [95]. PE reduced the D. magna reproduction in a dose-dependent manner at 5, 20 and 40 mg/L [83]. Smaller PE (17.23 ± 3.43 µm fragments) significantly reduced D. magna reproduction compared to larger PE (34.43 ± 13.09 µm fragments and 40–48 µm beads) [56]. Secondary PE had stronger effects on D. magna reproduction than primary microplastics [96]. PE decreased the number of broods produced by D. magna compared to PVC and PP [94]. PE and BaP had synergistic effects on reducing the D. magna reproduction [94]. PVC, PLA and PUR reduced the reproduction of D. magna within the range of 10–500 mg/L, and PVC had the greatest impacts followed by PLA and polyurethane (PUR). The 21-day EC 50 of PVC, PLA and polyurethane (PUR) for D. magna reproduction was 45.5, 122 and 236 mg/L [97], respectively. For other Cladocera species, 75 nm PS reduced the D. pulex reproduction within the range of 0.1–2 mg/L [58], whilst the 0.7 µm PS caused stronger effects on D. pulex and M. macrocopa reproduction than 1 µm PS, and M. macrocopa was more sensitive [84]. PE or mixtures of PE and Cd significantly reduced M. monogolica reproduction [85]. PE beads and polyester fibers reduced the reproduction of C. dubia in a dose-dependent manner within the range of 62.5–2000 μg/L, and polyester fibers caused greater impacts [24]. Primary microplastics and secondary PE reduced the reproduction of D. magna, D. pulex and C. dubia within the range of 0– 10 5 particles/mL, in which D. magna was the least sensitive species and C. dubia was the most sensitive species [98].
For Copepoda, 6 μm PS significantly reduced T. japonicus reproduction and fecundity at 0.23 mg/L [99]. Both 0.5 and 6 μm PS significantly reduced the fecundity of T. japonicus within the range of 0.125–25 mg/L, while 0.05 μm PS had no significant effect [69]. PS co-existed with dibutyl phthalate (DBP) and had antagonistic effects on T. japonicu reproduction [100]. Moreover, 0.05 μm PS reduced P. nana fecundity, followed by 0.5 μm PS, while 6 μm PS had no significant effect [89]. PS caused significant reproductive toxicity in Nitokra lacustris pacifca at 700 beads/mL [90]. PE led to the stress-induced spawning of Arctic Copepoda (Calanus finmarchicus and Calanus glacialis) at 20 particles/mL [101]. HDPE co-existed with CPF and produced significantly negative effects on A. tonsa reproduction [70]. PET significantly reduced the egg production of Parvocalanus crassirostris at 80,000 particles/mL [102]. For Amphipoda, PE significantly reduced the H. azteca neonate number at 5000 and 10,000 plastics/mL [74]. Tire wear particles significantly reduced the H. azteca reproductive output of 1000 particles/mL [75]. Additionally, for Anostraca, the polymer sphere reduced A. franciscana reproduction in a dose-dependent manner at 0.4, 0.8 and 1.6 mg/L [103].
Most papers showed that microplastics smaller than 500 microns had adverse effects on the life history of aquatic crustaceans. Smaller microplastics tend to have a greater effect on the survival of aquatic crustaceans than larger microplastics. The negative impacts of irregular microplastics (fibers, fragments) on the survival of aquatic crustaceans are greater than those of regular microplastics (spheres, beads). Primary or pristine microplastics have a greater negative impact on crustaceans’ survival than secondary or aged microplastics do. When microplastics co-exist with insecticides, herbicides, pesticides, anti-microbial agents, UV stabilizers and other contaminants, they have synergistic inhibiting effects on the survival of aquatic crustaceans. Generally, smaller microplastics have more significant negative effects on the growth and development of aquatic crustaceans than larger microplastics. Microfibers cause more negative effects on the growth and development of aquatic crustaceans than microspheres. When microplastics co-exist with pesticides and other contaminants, the negative effects on the growth and development of aquatic crustaceans are even greater. Smaller microplastics tend to have a higher reproductive toxicity than larger microplastics. The reproductive toxicity of fibers to aquatic crustaceans is higher than that of microspheres. When microplastics co-exist with herbicides, heavy metals and other contaminants, they have synergistic toxicity effects on the reproduction of aquatic crustaceans.

3. Effects of Microplastics on Behaviors of Aquatic Crustaceans

A total of 61 papers related to the effects of microplastics on aquatic crustacean behavior, including feeding behaviors (42 papers, 68.85%), swimming behaviors (21 papers, 34.43%), grazing behaviors (2 papers, 3.28%) and defense behaviors (1 paper, 1.64%) (Figure 2C). Of these, 22 papers focused on Cladocera (2 species), 15 papers on Copepoda (10 species), 9 papers on Amphipoda (6 species), 6 papers on Decapoda (5 species), 6 papers on Anostraca (2 species), 3 papers on Cirripedia (1 species) and 2 papers on Isopoda (2 species) (Figure 2D). The most studied aquatic crustaceans were D. magna, Calanus helgolandicus and A. amphitrite. The most extensively utilized types of microplastics were PS (34 papers, 55.74%), PE (14 papers, 22.95%), PET (3 papers, 4.92%) and PP (3 papers, 4.92%), whilst the most extensively utilized shapes were microspheres (21 papers, 34.43%), microbeads (16 papers, 26.23%), microfibers (8 papers, 13.11%) and fragments (5 papers, 8.20%).

3.1. Feeding Behaviors

For Copepoda, 0.5 and 10 μm PS could significantly reduce the Pseudodiaptomus annandalei feeding rate [104]. C. helgolandicus could avoid ingesting algae similar in size and/or shape to microplastics [105]. Nylon fibers led to a significant reduction in the algae intake of C. finmarchicus rather than nylon granules, which might work for C. finmarchicus avoiding microalgae that are similar in shape (i.e., chain-like Dunaliella tertiolecta) and size (i.e., Scripsiella trochoidea) to nylon fibers (10 × 30 μm) [106]. PE and oil had synergistic effects on inhibiting Calanus hyperboreus feeding [107]. Similarly, HDPE and CPF had more effects on reducing the A. tonsa feeding than each contaminant [70]. For Cladocera, PS could reduce the D. magna feeding capacity [108,109]. Primary PS decreased D. magna feeding efficiency more significantly than secondary PS [51]. PS at 40% of algal cells might have increased the algae intake of D. magna because D. magna expanded their filtration gapes when food availability declined [110]. Additionally, it has been found that D. magna might not distinguish similarly sized colorful PS and algae [110]. PET fibers affected algae consumption by D. magna more significantly than PP fibers [111]. Primary and secondary microplastics led to a 29% and 28% reduction in the food intake of D. magna [96]. For Decapoda, both 1 and 10 μm PS significantly reduced the feeding rate of N. awatschensis juveniles and adults at 5 × 10 5 particles/mL [61]. For Anostraca, PS significantly reduced the microalgal feeding by A. parthenogenetica at 100, 1000 and 10,000 particles/mL [112]. PS- NH 2 slightly increased the filtration rate in A. franciscana after 7 days while decreased the filtration rate after 14 days [91].

3.2. Swimming Behaviors

For Cladocera, 72.84 ± 6.81 nm PS reduced the swimming distances of D. magna in a dose-dependent manner within the range of 0–500 mg/L [53]. Both 20 and 200 nm PS-COOH significantly enhanced the D. magna swimming distance at 100 mg/L [113], and 1 and 10 μm PS increased D. magna swimming distance and speed at both 1.25 and 12.5 mg/L, which was considered to be avoidance behavior adopted by organisms to escape the polluted environment [81]. Plain PS and negative PS- NH 2 significantly reduced the swimming velocity and distance of D. magna, while PS-COOH and positive PS- NH 2 caused no significant effects [50]. PS co-existed with Gly induced greater effects on reducing D. magna swimming distance than single PS [53]. PS-COOH co-existed with Zn caused more effects on the frequency of movement of D. magna second antennae, thus affecting the swimming behavior [95]. PE reduced the D. magna hopping frequency in a dose-dependent manner within the range of 5–40 mg/L, which was related to the heartbeat rate reduction [83]. PE and BP-3 caused obvious damage to D. magna in terms of vertical swimming than single contaminants [114]. Polyamide (PA) could alleviate the decrease in velocity of Gammarus roeseli caused by phenanthrene (Phe), which might be related to the strong interaction between them [115]. For Decapoda, PS and PS-COOH affected the swimming speed, swimming time and swimming distance of N. japonica [63]. For Anostraca and Cirripedia, 0.1 µm PS beads significantly inhibited the A. franciscana and A. amphitrite swimming speeds at 1 and 10 mg/L [116], respectively.

3.3. Grazing and Defense Behaviors

For grazing behaviors, the PE spheres reduced the D. magna grazing rate on Chlorella vulgaris cells in a dose-dependent manner at 5, 20 and 40 mg/L, which was related to the hopping frequency reduction [83]. Dimethyl sulfide (DMS)-infused nylon fibers significantly reduced the C. helgolandicus grazing rates compared to virgin nylon fibers [117]. Additionally, for defense behaviors, the 4 mm PE at 25 particles/L significantly affected the attack and defense capabilities of Pagurus bernhardus, including effects on the attackers’ rapping intensity and strength, and weakening the defender’s ability to identify resources [118].
Microplastics exposure affects the feeding behaviors of aquatic crustaceans as these may be unable to distinguish similarly sized microplastics from food in most cases. When microplastics co-exist with contaminants such as oils and pesticides, they have a synergistic negative effect on the food intake of aquatic crustaceans. Primary microplastics reduce the feeding efficiency of aquatic crustaceans more than secondary microplastics. Many studies have shown that microplastics have negative impacts on the swimming behaviors of aquatic crustaceans, especially in terms of swimming speed and distance. The negative impact of the co-existence of microplastics and herbicides on the swimming behavior of aquatic crustaceans is higher than that of single contaminants. Microplastics reduced the grazing and defense behaviors of aquatic crustaceans.

4. Effects of Microplastics on Physiological Functions of Aquatic Crustaceans

There were 79 papers related to the physiological functions of microplastics on aquatic crustaceans, including oxidative damage (51 papers, 64.56%), neuromodulation (13 papers, 16.46%), energy regulation (13 papers, 16.46%), metabolic regulation (11 papers, 13.92%), respiratory regulation (7 papers, 8.86%), immunomodulation (7 papers, 8.86%) and intestinal physiology (8 papers, 10.13%) (Figure 2E). Among these, 31 papers focused on Decapoda (16 species), 26 papers on Cladocera (6 species), 11 papers on Anostraca (4 species), 7 papers on Copepoda (6 species), 3 papers on Amphipoda (4 species), 1 paper on Cirripedia (1 species) and 1 paper on Isopoda (1 species) (Figure 2F). The most concerned species among these aquatic crustaceans were D. magna, A. franciscana, D. pulex and L. vannamei. The most extensively utilized types of microplastics were PS (52 papers, 65.82%), PE (17 papers, 21.52%), PET (4 papers, 5.06%), PP (4 papers, 5.06%) and PVC (3 papers, 3.80%), whilst the most extensively utilized shapes were microspheres (33 papers, 41.77%), microbeads (19 papers, 24.05%), microfibers (5 papers, 6.33%) and fragments (4 papers, 5.06%).

4.1. Oxidative Damage

Most studies examined the oxidative stress caused by microplastics in aquatic crustaceans by measuring the lipid peroxidation (LPO), reactive oxygen species (ROS), total antioxidant capacity (TAC), H 2 O 2 and antioxidant enzyme activities including catalase (CAT), glutathione S-transferase (GST), glutathione peroxidase (GPx), glutathione reductase (GR), glutathione (GSH), superoxide dismutase (SOD), malondialdehyde (MDA), etc. For Decapoda, 5 µm PS caused the activities of SOD, GSH and GPx in Eriocheir sinensi, first increasing and then decreasing with the PS concentration, which increased within the range of 0.04–40 mg/L and might be related to the activation of an antioxidant system at low concentrations and the weakening of antioxidant activity at high concentrations [119]. Moreover, 75 nm PS significantly decreased SOD, CAT, se-glutathione peroxidase (GSH-Px) and glutathione S-transferase (GSH-ST) activities as well as GSH contents, while the increased LPO content all fell within the range of 5–40 mg/L. Additionally, this significantly increased H 2 O 2 and MDA contents in M. nipponense at 20 and 40 mg/L [62]. Between 10 and 22 µm PE clearly decreased the CAT activity in L. vannamei within the range of 0.1–1 μg/g in shrimp, increased the MDA content within the range of 0.2–1 μg/g in shrimp and decreased SOD activity at 0.2 and 1 μg/g in shrimp [66]. PS in the range of 0.5–1 µm and PE in the range of 30–150 µm significantly increased the antioxidant enzymes SOD, CAT, GST, GPx, GSH and LPO activities in M. rosenbergii in a dose-dependent manner at 1, 5 and 10 mg/100 g in food [87].
For Cladocera, PS raised the contents of total glutathione (T-GSH), GSH and oxidized glutathione (GSSG), as well as of ROS in D. magna within the ranges of 0–2 mg/L [120] and 0–500 mg/L [53] in a dose-dependent manner, respectively. Three-hundred nanometers of PS induced higher CAT and GPx activities in D. magna than the six-hundred-nanometer ones [121]. Additionally, 0.05 and 0.5 μm PS significantly increased the MDA concentration in Diaphanosoma celebensis while 6 μm PS caused moderate alterations [122]. Plain PS generated greater oxidative stress in D. magna than PS-COOH and PS- NH 2 [50], while amine-modified PS and carboxyl-modified PS both caused more severe oxidative damage to D. magna than PS [123]. PE significantly enhanced the ROS, TAC and LPO in D. magna in a dose-dependent manner within the range of 0.1–1 mg/L [55]. PE and BP-3 exhibited significantly synergistic interactions on the increasing ROS, TAC and LPO of D. magna [55]. Comparing PS and PE, 0.3–9 µm PE induced higher enzymes activities than 300 nm PS. Both PS (300 nm and 600 nm) and PE (0.3–9 µm) enhanced the oxidative stress of silver (Ag) by increasing the enzyme activity in D. magna [121].
For Anostraca, PS significantly increased the CAT activity in A. franciscana within the range of 0.001–1 mg/L [116]. PS- NH 2 significantly decreased the antioxidant enzyme GST and CAT activities in A. franciscana at 1 mg/L [91]. PS increased the ROS level in A. salina [124]. Additionally, PS-COOH could alleviate the oxidative damage in A. salina caused by nano- TiO 2 [73]. For Copepoda, 50 nm PS induced higher ROS in T. japonicus than 10 μm PS [26]. However, 0.05 μm PS significantly increased the ROS levels as well as GPx, GR, GST and SOD activities in P. nana, followed by 0.5 and 6 μm PS [89]. For Cirripedia, 0.1 µm PS significantly decreased the CAT activities in A. amphitrite at 0.001 mg/L and significantly increased it at 0.1 and 1 mg/L [116].

4.2. Neuromodulation

Neuromodulation could be measured by enzymes activities such as acetylcholineesterase (AChE), pseudocholinesterase (PChE), cholinesterase (ChE) and carboxylesterase (CbE). For Decapoda, PS could affect the neural activity by AChE activity reduction in Charybdis japonica [29]. Five-nanometer PS significantly reduced the AChE activity in E. sinensis in a dose-dependent manner within the range of 0–40 mg/L [119]. Additionally, PS could affect the changes in AChE activity caused by heavy metals (arsenic (As), Cd, Cu, Pb and Zn) in both N. awatschensis juveniles and adults [125]. For Anostraca, PS significantly decreased the AChE activity in A. franciscana at 0.001 and 0.01 mg/L and increased the PChE activity at 0.01 and 0.1 mg/L [116]. PS- NH 2 significantly reduced the ChE and CbE activities in A. franciscana at 1 mg/L [91]. Polymer spheres significantly increased the CbE and ChE activities in A. franciscana nauplii at 1.6 mg/L and significantly increased the CbE and ChE activities in A. franciscana juveniles at 0.4 and 1.6 mg/L [126]. For Cladocera, plain PS suspension increased the AChE activity, while the functionalized PS significantly decreased the AChE activity in D. magna [50]. One-micrometer PS affected AChE activity in M. macrocopa within the range of 0–500 μg/L after 7 days [127]. For Cirripedia, PS significantly increased the AChE and PChE activities in A. amphitrite within the range of 0.001–0.1 mg/L, especially at 0.001 mg/L [116].

4.3. Energy Regulation

The carbohydrate storage [128], fatty acid content and composition [129], essential amino acid content [130], carbon budget [131], energy balance [88], lipid stores [132] and protein content [133] could be used to evaluate the energy regulation. PS beads increased the energetic losses in C. helgolandicus [131], PS spheres caused changes in fatty acids and essential amino acids in L. vannamei [130] and PS fragments had more significant effects on the reduction in carbohydrate and protein energy storage on D. magna than beads [56]. Moreover, 300 μg/L PE more significantly reduced the ratios of protein, carbohydrates, lipids and caloric contents in M. monogolica than 100 μg/L PE [85], and mixtures of PE and Cd caused a more obvious energy drop than PE [85]. The PP fibers affected the energy balance in C. maenas [88] and reduced the stored lipids in Nephrops norvegicus [132]. PET significantly increased the energy consumption in D. magna when co-existed with Ag or Ag NO 3 . Nylon fibers induced the higher lipid accumulation than nylon granules in C. finmarchicus [106].

4.4. Metabolic Regulation

The metabolic regulation of microplastics on aquatic crustaceans could be detected by metabolic enzymes activity (such as glutamic-oxaloacetic transaminase (GOT) and glutamic-pyruvic transaminase (GPT) [87]), excretion rates, metabolic rate [132], lipid metabolism [134], carbohydrate metabolism [128], digestive enzyme activity [135], etc. For Decapoda, 75 nm PS significantly affected the energy metabolism-related substance content and energy metabolism-related enzyme activity (glucose metabolism and lipid metabolism) in M. nipponense in dose-dependent manners within the range of 5–40 mg/L [60]. Two-hundred nanometer PS reduced the lipase (LPS) and acetyl-CoA carboxylase (ACC) activities in Cherax quadricarinatus at 0.5 and 5 mg/L [136], respectively. The PS co-existed with bisphenol A (BPA) more significantlyaffected the metabolism in L. vannamei than single contaminant [137]. PE and PS significantly reduced the metabolic enzymes of GOT and GPT activities in M. rosenbergii in a dose-dependent manner at 1, 5 and 10 mg/100 g in food [87].

4.5. Respiratory Regulation

The effects of microplastics on the respiration regulation in aquatic crustaceans could be detected by changes in respiration rate. For Copepoda, polystyrene reduced the respiration rates in Centropages typicus and Acartia clausi by 3.4 and 2.2 times, respectively [138]. Moreover, 6, 12 and 26 µm polystyrene could significantly reduce the C. helgolandicus respiration rate [139]. For Decapoda, PET fibers could decrease the respiration rates on later larval Homarus americanus [140]. PS could make C. maenas have a higher oxygen consumption [141]. PS co-existed with BPA caused more effects on L. vannamei respiration than single contaminant [137]. For Amphipoda, PMMA reduced the Gammarus pulex respiration rate at 0.52, 26.12 and 104.48 particles/ cm 2 [142].

4.6. Immunomodulation

Immunomodulation could be tested by immune-related activities [62], immune-related genes expression [65] and the blood cell number [143]. For Decapoda, 75 nm PS induced reductions in the immune-related enzymes acid phosphatase (ACP), alkaline phosphatase (AKP), lysozyme (LZM) and phenoloxidase (PO) activities of M. nipponense within the range of 5–40 mg/L [62]. The 5 µm PS affected ACP, AKP, LZM and PO activities in the hemolymph and hepatopancreas of E. sinensis within the range of 0–40 mg/L, indicating that low-concentrations of PS might affect the immune response, and high concentrations of PS negatively influenced all aspects of innate immunity [144]. The 5 μm PE significantly increased the immune-related genes’ relative expression in L. vannamei at 500 and 5000 μg/L compared to 50 μg/L PE [65].

4.7. Intestinal Physiology

The intestinal physiology could be observed by detecting the intestinal microbiota of aquatic crustaceans. For Decapoda, PS induced the intestinal microbial imbalance in E. sinensis within the range of 0.04–40 mg/L [144]. PE induced the intestinal microbial imbalance in L. vannamei in a dose-dependent manner within the range of 50–5000 μg/L [65]. PE, PS, PP, PVC and polytetrafluoroethylene (PTFE) differently affected the stability of intestinal microbiota in L. vannamei and changed the gut microbiome in juveniles [134]. For Anostraca, PE has more serious disruption to the intestinal microbiota of A. parthenogenetica and a larger suppression of the growth rate compared with PS [92].
Most papers showed that microplastics could induce oxidative stress in aquatic crustaceans. In general, the oxidative stress of aquatic crustaceans caused by smaller microplastics is higher than that caused by larger microplastics. Microplastics co-existing with UV absorbers and other contaminants could cause synergistic effects on oxidative stress in aquatic crustaceans. Microplastics caused neurotoxicity in aquatic crustaceans. Microplastics affect the energy status of aquatic crustaceans, and the co-existence of microplastics and heavy metals has a greater impact on the energy consumption of aquatic crustaceans. Microplastics and other contaminants could cause synergistic effects on the metabolism and respiration of aquatic crustaceans. Microplastics exposure affected the stability of the intestinal microflora of aquatic crustaceans to varying degrees.

5. Response Mechanisms of Aquatic Crustaceans to Microplastics Stress

5.1. Oxidation Mechanism

Oxidative stress is one of the response mechanisms of aquatic crustaceans to microplastics stress. Oxidative stress frequently affects the cell membrane first, and transmits the stress signal to functional proteins via some signal transduction pathways such as mitogen-active protein kinases (MAPK), Jak-STAT, mTOR and Foxo, and then affects biological processes such as cell growth and proliferation. For example, PS permeated into the cell membrane with high bioavailability, which induced the cell damage, leading to the oxidative stress response of crustaceans. This is the main reason for the cell growth rate and proliferation inhibition in crustaceans exposed to PS [132]. PS induced oxidative stress in E. sinensis by affecting the MAPK signaling pathway [119]. The PS-caused ROS activates signaling in MAPK pathways (like p38 and p-JNK), resulting in lethal and adverse behavioral effects on D. magna. PS-COOH and negative PS- NH 2 might interact with cell surface receptor to activate MAPK by inducing p-p38 and p-JNK and stimulate the antioxidant system in the absence of ROS induction [50]. Additionally, for nanoplastics, nano-sized PS induced significant oxidative stress to aquatic crustaceans by penetrating the cellular membrane, causing more cellular damage than larger microplastics. These effects could be shown by the transcriptional modulation of antioxidant-related genes and enzyme activities [122]. Nano-sized PS induced D. pulex oxidative stress, affecting the arachidonic acid metabolism, glutathione metabolism and porphyrin and chlorophyll metabolism [145]. Nano-sized PS could induce a pronounced overproduction of ROS, leading to the inhibitions of D. pulex growth and reproduction through cell damage [146].

5.2. Metabolic Mechanism

The metabolic mechanism was another mechanism of aquatic crustaceans’ response to microplastics stress. Microplastics could affect the metabolism of aquatic crustaceans by affecting the adenosine monophosphate-activated protein kinase (AMPK) activation and then adenosine triphosphate (ATP) decomposition, affecting the metabolic mechanism and thus affecting various metabolic processes, energy status and other biological processes. In brief, the AMPK could be detected as activated, when the balance between ATP, adenosine diphosphate (ADP) and adenosine monophosphate (AMP) was destroyed. AMPK activation provided energy and helped organisms cope with stress through the synthesis of antioxidants and cellular stress responses [147]. Once activated by energy stressors, AMPK triggered metabolic changes by activating the catabolic pathways that generate ATP while shutting down anabolic pathways and other ATP-consuming processes that were not important for survival [148]. Microplastics could affect the various metabolic processes of aquatic crustaceans, such as lipid metabolism, glucose metabolism, etc. PS significantly reduced the expression of fatty acid metabolism-related genes (FAD6 and FABP) in C. quadricarinatus, significantly increased the activity of lipase related to lipolysis in hepatopancreas, and increased that of fatty acid synthase related to fat synthesis and decreased that of acetyl-CoA carboxylase. The significant increased in lipid transport-related low-density lipoprotein suggests that lipolysis was superior to lipid synthesis [136]. PS could reduce the lipid content of juvenile shrimp by reducing the ability of M. nipponense to digest, transport and synthesize lipids. By down-regulating the expression of genes related to lipid metabolism, the PS reduced the activity of related enzymes, weakened the ability to digest, transport and synthesize lipids, resulting in the reduction in the lipid content in M. nipponense [60]. PS could cause glycolytic process inhibition, increase the anaerobic glucose metabolism, cause a shortage of energy supplies and lead to a shift from aerobic to anaerobic metabolism in M. nipponense [60]. Additionally, PS regulated the ion transport and energy metabolism-related enzymes and gene expression in M. nipponense, impacting the ion transport and damage on cell osmotic regulation [149]. PS led to an increase in several cellular biosynthetic processes, which in turn, due to trade-offs, reduced the energy storage, thus affecting the survival and reproduction of T. japonicus [99]. PS induced the disruption of the defense mechanism, as indicated by the abundance in ATP-binding cassette (ABC) family proteins, which can transfer harmful compounds out of cells [150].

5.3. Immune Mechanism

Microplastics also activate the immune mechanism of aquatic crustaceans. PS could activate the immune system of juvenile M. nipponense, stimulate the release of LZM from lysosomes and promote the release of hydrolytic enzymes AKP and ACP to resist immune stress, and high concentrations of PS or long-term exposure impaired lysosomal degradation and impeded phagocytosis by pathogens, inhibited the release of ACP and AKP in lysosomes and affected immune defense [62]. PS could stimulate cell apoptosis, which is an important regulatory feature of innate immune response and the most common form of death in immune cells, and might be through endocytosis across the cell membrane to activate the apoptosis pathway in M. nipponense [149]. PS impacted the contents and activities of most immune-related factors in hemolymph, blood cells, pancreas and liver of E. sinensis [144]. PS, PE, PP, PVC and PTFE differently affected the pathways and expression of immune-related proteins in L. vannamei. PS might influence shrimp’s antioxidant status and damage shrimp’s immunity in recognizing pathogenic molecules PE might also damage shrimp’s immunity by recognizing pathogenic molecules and affect the stability of shrimp’s extracellular matrix. PVC might influence shrimp’s immune homeostasis, antioxidant status and immunity in recognizing pathogenic molecules. PTFE induced an immune response [134].

6. Conclusions and Outlook

Most papers indicated that smaller microplastics tended to have greater effects on the life histories of aquatic crustaceans than those of larger microplastics in general. Irregular microplastics often had more negative impacts on the life histories of aquatic crustaceans than regular ones. Generally, microplastics co-existed with other contaminants had synergistic effects on the life history of aquatic crustaceans. Additionally, primary or pristine microplastics were found to have a greater negative impact on crustaceans’ survival than secondary or aged microplastics did. Microplastics caused negative effects on the feeding, swimming, grazing and defense behaviors of aquatic crustaceans. Microplastics co-existing with other contaminants led to more negative effects on feeding and swimming behaviors. Additionally, primary microplastics reduced the feeding efficiency of aquatic crustaceans more than secondary ones. Microplastics affected several physiological functions of aquatic crustaceans. Microplastics co-existed with other contaminants caused more negative effects on oxidative stress, metabolic regulation, metabolism and respiration in aquatic crustaceans. Smaller microplastics had more effects on the oxidative stress of aquatic crustaceans than larger microplastics. Oxidative stress frequently affected the cell membrane first, and transmitted the stress signal to functional proteins via some signal transduction pathways and then affected the biological processes such as cell growth and proliferation. Microplastics affected the metabolism of aquatic crustaceans, thus affecting organisms. Microplastics could also activate the immune mechanism of aquatic crustaceans differently and cause an immune response.
The review discovers that the research performed by studies on the effects of microplastics of aquatic crustaceans is incomplete and some problems need to be solved. Insufficient types of microplastics were used in the study. There were more studies on PS and PE, while there were less studies on other types of microplastics. There have been many studies on native microplastics, but few on aged or weathered microplastics. In this regard, we should expand the research on the types of microplastics, which should not only be limited to the available microplastics, but also pay more attention to microplastics affected by aging and weathering processes. It was found that the size ranges of microplastics are relatively limited and their shapes are relatively regular, in addition to being quite different from the shapes of the microplastics existing in the environment. In view of this problem, it is necessary to study the sizes and shapes of microplastics that are similar to those in the environment, and pay further attention to the impacts of irregularly shaped microplastics on aquatic crustaceans. It is also found that the test concentrations are generally higher than those in the environment. Therefore, we should strengthen the long-term impacts of microplastics with an environmental concentration on aquatic crustaceans. This review finds that the research on the impacts of microplastics co-existed with other contaminants in aquatic crustaceans is insufficient, and should be further strengthened. This review finds that the species of aquatic crustaceans used in studies are relatively limited, with more research focusing on Cladocera, especially D. magna. Therefore, we should pay more attention to the effects on more types of aquatic crustaceans, including different species and different life stages, and the exposure time should be extended to further observe the intergenerational effects and biohazards of microplastics. In addition, researchers should further research the mechanisms of biotoxicity in microplastics.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/ijms24065523/s1.

Author Contributions

Literature search, conceptualization, S.Z. and H.W.; screen, review, extract and analyze literatures, S.Z.; write the first draft of the manuscript, S.Z. and H.W.; review and revise the manuscript and approved the final draft, J.H. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (22276052).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

I thank all the colleagues who participated in this work.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Jambeck, J.R.; Geyer, R.; Wilcox, C.; Siegler, T.R.; Perryman, M.; Andrady, A.; Narayan, R.; Law, K.L. Plastic waste inputs from land into the ocean. Science 2015, 347, 768–771. [Google Scholar] [CrossRef]
  2. Geyer, R.; Jambeck, J.R.; Law, K.L. Production, use, and fate of all plastics ever made. Sci. Adv. 2017, 3, e1700782. [Google Scholar] [CrossRef] [Green Version]
  3. Enfrin, M.; Lee, J.; Gibert, Y.; Basheer, F.; Kong, L.; Dumée, L.F. Release of hazardous nanoplastic contaminants due to microplastics fragmentation under shear stress forces. J. Hazard. Mater. 2020, 384, 121393. [Google Scholar] [CrossRef] [PubMed]
  4. Lambert, S.; Wagner, M. Characterisation of nanoplastics during the degradation of polystyrene. Chemosphere 2016, 145, 265–268. [Google Scholar] [CrossRef] [Green Version]
  5. Dawson, A.L.; Kawaguchi, S.; King, C.K.; Townsend, K.A.; King, R.; Huston, W.M.; Bengtson Nash, S.M. Turning microplastics into nanoplastics through digestive fragmentation by Antarctic krill. Nat. Commun. 2018, 9, 1001. [Google Scholar] [CrossRef] [PubMed]
  6. Thompson, R.C.; Olsen, Y.; Mitchell, R.P.; Davis, A.; Rowland, S.J.; John, A.W.; McGonigle, D.; Russell, A.E. Lost at sea: Where is all the plastic? Science 2004, 304, 838. [Google Scholar] [CrossRef]
  7. EFSA Panel on Contaminants in the Food Chain (CONTAM). Presence of microplastics and nanoplastics in food, with particular focus on seafood. EFSA J. 2016, 14, e04501. [Google Scholar] [CrossRef] [Green Version]
  8. Auta, H.S.; Emenike, C.U.; Fauziah, S.H. Distribution and importance of microplastics in the marine environment: A review of the sources, fate, effects, and potential solutions. Environ. Int. 2017, 102, 165–176. [Google Scholar] [CrossRef] [PubMed]
  9. Cozar, A.; Echevarria, F.; Gonzalez-Gordillo, J.I.; Irigoien, X.; Ubeda, B.; Hernandez-Leon, S.; Palma, A.T.; Navarro, S.; Garcia-de-Lomas, J.; Ruiz, A.; et al. Plastic debris in the open ocean. Proc. Natl. Acad. Sci. USA 2014, 111, 10239–10244. [Google Scholar] [CrossRef] [Green Version]
  10. Van Cauwenberghe, L.; Vanreusel, A.; Mees, J.; Janssen, C.R. Microplastic pollution in deep-sea sediments. Environ. Pollut. 2013, 182, 495–499. [Google Scholar] [CrossRef]
  11. Horton, A.A.; Walton, A.; Spurgeon, D.J.; Lahive, E.; Svendsen, C. Microplastics in freshwater and terrestrial environments: Evaluating the current understanding to identify the knowledge gaps and future research priorities. Sci. Total Environ. 2017, 586, 127–141. [Google Scholar] [CrossRef] [Green Version]
  12. Chia, R.W.; Lee, J.; Kim, H.; Jang, J. Microplastic pollution in soil and groundwater: A review. Environ. Chem. Lett. 2021, 19, 4211–4224. [Google Scholar] [CrossRef]
  13. Yonkos, L.T.; Friedel, E.A.; Perez-Reyes, A.C.; Ghosal, S.; Arthur, C.D. Microplastics in four estuarine rivers in the Chesapeake bay, U.S.A. Environ. Sci. Technol. 2014, 48, 14195–14202. [Google Scholar] [CrossRef] [PubMed]
  14. Waller, C.L.; Griffiths, H.J.; Waluda, C.M.; Thorpe, S.E.; Loaiza, I.; Moreno, B.; Pacherres, C.O.; Hughes, K.A. Microplastics in the Antarctic marine system: An emerging area of research. Sci. Total Environ. 2017, 598, 220–227. [Google Scholar] [CrossRef] [Green Version]
  15. Koelmans, A.A.; Mohamed Nor, N.H.; Hermsen, E.; Kooi, M.; Mintenig, S.M.; De France, J. Microplastics in freshwaters and drinking water: Critical review and assessment of data quality. Water Res. 2019, 155, 410–422. [Google Scholar] [CrossRef] [PubMed]
  16. Codina-García, M.; Militão, T.; Moreno, J.; González-Solís, J. Plastic debris in Mediterranean seabirds. Mar. Pollut. Bull. 2013, 77, 220–226. [Google Scholar] [CrossRef]
  17. Lynch, J.M. Quantities of marine debris ingested by sea turtles: Global meta-analysis highlights need for standardized data reporting methods and reveals relative risk. Environ. Sci. Technol. 2018, 52, 12026–12038. [Google Scholar] [CrossRef]
  18. Cole, M.; Lindeque, P.; Fileman, E.; Halsband, C.; Goodhead, R.; Moger, J.; Galloway, T.S. Microplastic ingestion by zooplankton. Environ. Sci. Technol. 2013, 47, 6646–6655. [Google Scholar] [CrossRef] [PubMed]
  19. Foekema, E.M.; De Gruijter, C.; Mergia, M.T.; van Franeker, J.A.; Murk, A.J.; Koelmans, A.A. Plastic in North sea fish. Environ. Sci. Technol. 2013, 47, 8818–8824. [Google Scholar] [CrossRef]
  20. Lusher, A.L.; Hernandez-Milian, G.; O’Brien, J.; Berrow, S.; O’Connor, I.; Officer, R. Microplastic and macroplastic ingestion by a deep diving, oceanic cetacean: The True’s beaked whale Mesoplodon mirus. Environ. Pollut. 2015, 199, 185–191. [Google Scholar] [CrossRef]
  21. Welden, N.A.C.; Cowie, P.R. Environment and gut morphology influence microplastic retention in langoustine, Nephrops norvegicus. Environ. Pollut. 2016, 214, 859–865. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Li, J.; Yang, D.; Li, L.; Jabeen, K.; Shi, H. Microplastics in commercial bivalves from China. Environ. Pollut. 2015, 207, 190–195. [Google Scholar] [CrossRef] [PubMed]
  23. Nasser, F.; Lynch, I. Secreted protein eco-corona mediates uptake and impacts of polystyrene nanoparticles on Daphnia magna. J. Proteom. 2016, 137, 45–51. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Ziajahromi, S.; Kumar, A.; Neale, P.A.; Leusch, F.D.L. Impact of microplastic beads and fibers on waterflea (Ceriodaphnia dubia) survival, growth, and reproduction: Implications of single and mixture exposures. Environ. Sci. Technol. 2017, 51, 13397–13406. [Google Scholar] [CrossRef] [Green Version]
  25. Besseling, E.; Wang, B.; Lürling, M.; Koelmans, A.A. Nanoplastic affects growth of S. obliquus and reproduction of D. magna. Environ. Sci. Technol. 2014, 48, 12336–12343. [Google Scholar] [CrossRef]
  26. Choi, J.S.; Hong, S.H.; Park, J. Evaluation of microplastic toxicity in accordance with different sizes and exposure times in the marine copepod Tigriopus japonicus. Mar. Environ. Res. 2020, 153, 104838. [Google Scholar] [CrossRef]
  27. Mazurais, D.; Ernande, B.; Quazuguel, P.; Severe, A.; Huelvan, C.; Madec, L.; Mouchel, O.; Soudant, P.; Robbens, J.; Huvet, A.; et al. Evaluation of the impact of polyethylene microbeads ingestion in European sea bass (Dicentrarchus labrax) larvae. Mar. Environ. Res. 2015, 112, 78–85. [Google Scholar] [CrossRef] [Green Version]
  28. Xu, E.G.; Cheong, R.S.; Liu, L.; Hernandez, L.M.; Azimzada, A.; Bayen, S.; Tufenkji, N. Primary and secondary plastic particles exhibit limited acute toxicity but chronic effects on Daphnia magna. Environ. Sci. Technol. 2020, 54, 6859–6868. [Google Scholar] [CrossRef]
  29. Wang, T.; Hu, M.; Xu, G.; Shi, H.; Leung, J.Y.S.; Wang, Y. Microplastic accumulation via trophic transfer: Can a predatory crab counter the adverse effects of microplastics by body defence? Sci. Total Environ. 2021, 754, 142099. [Google Scholar] [CrossRef]
  30. Zou, W.; Xia, M.; Jiang, K.; Cao, Z.; Zhang, X.; Hu, X. Photo-oxidative degradation mitigated the developmental toxicity of polyamide microplastics to zebrafish larvae by modulating macrophage-triggered proinflammatory responses and apoptosis. Environ. Sci. Technol. 2020, 54, 13888–13898. [Google Scholar] [CrossRef]
  31. Setälä, O.; Fleming-Lehtinen, V.; Lehtiniemi, M. Ingestion and transfer of microplastics in the planktonic food web. Environ. Pollut. 2014, 185, 77–83. [Google Scholar] [CrossRef]
  32. Mateos-Cárdenas, A.; Scott, D.T.; Seitmaganbetova, G.; van Pelt Frank, N.A.M.; John, O.; Jansen, M.A.K. Polyethylene microplastics adhere to Lemna minor (L.), yet have no effects on plant growth or feeding by Gammarus duebeni (Lillj.). Sci. Total Environ. 2019, 689, 413–421. [Google Scholar] [CrossRef]
  33. Costa, E.; Piazza, V.; Lavorano, S.; Faimali, M.; Garaventa, F.; Gambardella, C. Trophic transfer of microplastics from copepods to jellyfish in the marine environment. Front. Environ. Sci. 2020, 8, 571732. [Google Scholar] [CrossRef]
  34. Elizalde-Velázquez, A.; Carcano, A.M.; Crago, J.; Green, M.J.; Shah, S.A.; Cañas-Carrell, J.E. Translocation, trophic transfer, accumulation and depuration of polystyrene microplastics in Daphnia magna and Pimephales promelas. Environ. Pollut. 2020, 259, 113937. [Google Scholar] [CrossRef]
  35. Mattsson, K.; Johnson, E.V.; Malmendal, A.; Linse, S.; Hansson, L.; Cedervall, T. Brain damage and behavioural disorders in fish induced by plastic nanoparticles delivered through the food chain. Sci. Rep. 2017, 7, 11452. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Hasegawa, T.; Nakaoka, M. Trophic transfer of microplastics from mysids to fish greatly exceeds direct ingestion from the water column. Environ. Pollut. 2021, 273, 116468. [Google Scholar] [CrossRef] [PubMed]
  37. Dodson, S.I.; Frey, D.G. 21-Cladocera and other Branchiopoda. In Ecology and Classification of North American Freshwater Invertebrates, 2nd ed.; Thorp, J.H., Covich, A.P., Eds.; Academic Press: San Diego, CA, USA, 2001; pp. 849–913. [Google Scholar]
  38. Tkaczyk, A.; Bownik, A.; Dudka, J.; Kowal, K.; Ślaska, B. Daphnia magna model in the toxicity assessment of pharmaceuticals: A review. Sci. Total Environ. 2021, 763, 143038. [Google Scholar] [CrossRef] [PubMed]
  39. Vogt, G. Cytology, function and dynamics of stem and progenitor cells in decapod crustaceans. Biol. Rev. 2022, 97, 817–850. [Google Scholar] [CrossRef]
  40. Yin, J.; Li, J.; Craig, N.J.; Su, L. Microplastic pollution in wild populations of decapod crustaceans: A review. Chemosphere 2022, 291, 132985. [Google Scholar] [CrossRef]
  41. Raisuddin, S.; Kwok, K.W.H.; Leung, K.M.Y.; Schlenk, D.; Lee, J. The copepod Tigriopus: A promising marine model organism for ecotoxicology and environmental genomics. Aquat. Toxicol. 2007, 83, 161–173. [Google Scholar] [CrossRef]
  42. Brendonck, L.; Rogers, D.C.; Olesen, J.; Weeks, S.; Hoeh, W.R. Global diversity of large branchiopods (Crustacea: Branchiopoda) in freshwater. Hydrobiologia 2008, 595, 167–176. [Google Scholar] [CrossRef]
  43. Kunz, P.Y.; Kienle, C.; Gerhardt, A. Gammarus spp. in aquatic ecotoxicology and water quality assessment: Toward integrated multilevel tests. Rev. Environ. Contam. Toxicol. 2010, 205, 1–76. [Google Scholar] [CrossRef]
  44. Pérez-Losada, M.; Høeg, J.T.; Crandall, K.A. Unraveling the evolutionary radiation of the thoracican barnacles using molecular and morphological evidence: A comparison of several divergence time estimation approaches. Syst. Biol. 2004, 53, 244–264. [Google Scholar] [CrossRef]
  45. Rumbold, C.; Meloni, M.; Doti, B.; Correa, N.; Albano, M.; Sylvester, F.; Obenat, S. Two new nonindigenous isopods in the Southwestern Atlantic: Simultaneous assessment of population status and shipping transport vector. J. Sea Res. 2018, 138, 1–7. [Google Scholar] [CrossRef] [Green Version]
  46. Fadare, O.O.; Wan, B.; Liu, K.; Yang, Y.; Zhao, L.; Guo, L. Eco-corona vs protein corona: Effects of humic substances on corona formation and nanoplastic particle toxicity in Daphnia magna. Environ. Sci. Technol. 2020, 54, 8001–8009. [Google Scholar] [CrossRef]
  47. Fadare, O.O.; Wan, B.; Guo, L.; Xin, Y.; Qin, W.; Yang, Y. Humic acid alleviates the toxicity of polystyrene nanoplastic particles to Daphnia magna. Environ. Sci. Nano 2019, 6, 1466–1477. [Google Scholar] [CrossRef]
  48. Lin, H.; Yuan, Y.; Jiang, X.; Zou, J.; Xia, X.; Luo, S. Bioavailability quantification and uptake mechanisms of pyrene associated with different-sized microplastics to Daphnia magna. Sci. Total Environ. 2021, 797, 149201. [Google Scholar] [CrossRef] [PubMed]
  49. Saavedra, J.; Stoll, S.; Slaveykova, V.I. Influence of nanoplastic surface charge on eco-corona formation, aggregation and toxicity to freshwater zooplankton. Environ. Pollut. 2019, 252, 715–722. [Google Scholar] [CrossRef] [Green Version]
  50. Lin, W.; Jiang, R.; Hu, S.; Xiao, X.; Wu, J.; Wei, S.; Xiong, Y.; Ouyang, G. Investigating the toxicities of different functionalized polystyrene nanoplastics on Daphnia magna. Ecotoxicol. Environ. Saf. 2019, 180, 509–516. [Google Scholar] [CrossRef]
  51. Liu, Z.; Zhu, Y.; Lv, S.; Shi, Y.; Dong, S.; Yan, D.; Zhu, X.; Peng, R.; Keller, A.A.; Huang, Y. Quantifying the dynamics of polystyrene microplastics UV-aging process. Environ. Sci. Technol. Lett. 2022, 9, 50–56. [Google Scholar] [CrossRef]
  52. Felten, V.; Toumi, H.; Masfaraud, J.; Billoir, E.; Camara, B.I.; Férard, J. Microplastics enhance Daphnia magna sensitivity to the pyrethroid insecticide deltamethrin: Effects on life history traits. Sci. Total Environ. 2020, 714, 136567. [Google Scholar] [CrossRef] [PubMed]
  53. Nogueira, D.J.; Silva, A.C.D.O.; Da Silva, M.L.N.; Vicentini, D.S.; Matias, W.G. Individual and combined multigenerational effects induced by polystyrene nanoplastic and glyphosate in Daphnia magna (Strauss, 1820). Sci. Total Environ. 2022, 811, 151360. [Google Scholar] [CrossRef]
  54. Yuan, W.; Zhou, Y.; Chen, Y.; Liu, X.; Wang, J. Toxicological effects of microplastics and heavy metals on the Daphnia magna. Sci. Total Environ. 2020, 746, 141254. [Google Scholar] [CrossRef] [PubMed]
  55. Na, J.; Song, J.; Achar, J.C.; Jung, J. Synergistic effect of microplastic fragments and benzophenone-3 additives on lethal and sublethal Daphnia magna toxicity. J. Hazard. Mater. 2021, 402, 123845. [Google Scholar] [CrossRef] [PubMed]
  56. An, D.; Na, J.; Song, J.; Jung, J. Size-dependent chronic toxicity of fragmented polyethylene microplastics to Daphnia magna. Chemosphere 2021, 271, 129591. [Google Scholar] [CrossRef] [PubMed]
  57. Amariei, G.; Rosal, R.; Fernández-Piñas, F.; Koelmans, A.A. Negative food dilution and positive biofilm carrier effects of microplastic ingestion by D. magna cause tipping points at the population level. Environ. Pollut. 2022, 294, 118622. [Google Scholar] [CrossRef]
  58. Liu, Z.; Yu, P.; Cai, M.; Wu, D.; Zhang, M.; Huang, Y.; Zhao, Y. Polystyrene nanoplastic exposure induces immobilization, reproduction, and stress defense in the freshwater cladoceran Daphnia pulex. Chemosphere 2019, 215, 74–81. [Google Scholar] [CrossRef]
  59. Jaikumar, G.; Baas, J.; Brun, N.R.; Vijver, M.G.; Bosker, T. Acute sensitivity of three Cladoceran species to different types of microplastics in combination with thermal stress. Environ. Pollut. 2018, 239, 733–740. [Google Scholar] [CrossRef] [Green Version]
  60. Li, Y.; Liu, Z.; Yang, Y.; Jiang, Q.; Wu, D.; Huang, Y.; Jiao, Y.; Chen, Q.; Huang, Y.; Zhao, Y. Effects of nanoplastics on energy metabolism in the oriental river prawn (Macrobrachium nipponense). Environ. Pollut. 2021, 268, 115890. [Google Scholar] [CrossRef]
  61. Lee, D.; Lee, S.; Rhee, J. Consistent exposure to microplastics induces age-specific physiological and biochemical changes in a marine mysid. Mar. Pollut. Bull. 2021, 162, 111850. [Google Scholar] [CrossRef]
  62. Li, Y.; Liu, Z.; Li, M.; Jiang, Q.; Wu, D.; Huang, Y.; Jiao, Y.; Zhang, M.; Zhao, Y. Effects of nanoplastics on antioxidant and immune enzyme activities and related gene expression in juvenile Macrobrachium nipponense. J. Hazard. Mater. 2020, 398, 122990. [Google Scholar] [CrossRef]
  63. Wang, X.; Liu, L.; Zheng, H.; Wang, M.; Fu, Y.; Luo, X.; Li, F.; Wang, Z. Polystyrene microplastics impaired the feeding and swimming behavior of mysid shrimp Neomysis japonica. Mar. Pollut. Bull. 2020, 150, 110660. [Google Scholar] [CrossRef] [PubMed]
  64. Wang, Z.; Fan, L.; Wang, J.; Zhou, J.; Ye, Q.; Zhang, L.; Xu, G.; Zou, J. Impacts of microplastics on three different juvenile shrimps: Investigating the organism response distinction. Environ. Res. 2021, 198, 110466. [Google Scholar] [CrossRef] [PubMed]
  65. Wang, Z.; Fan, L.; Wang, J.; Xie, S.; Zhang, C.; Zhou, J.; Zhang, L.; Xu, G.; Zou, J. Insight into the immune and microbial response of the white-leg shrimp Litopenaeus vannamei to microplastics. Mar. Environ. Res. 2021, 169, 105377. [Google Scholar] [CrossRef]
  66. Hsieh, S.; Wu, Y.; Xu, R.; Chen, Y.; Chen, C.; Singhania, R.R.; Dong, C. Effect of polyethylene microplastics on oxidative stress and histopathology damages in Litopenaeus vannamei. Environ. Pollut. 2021, 288, 117800. [Google Scholar] [CrossRef]
  67. Gray, A.D.; Weinstein, J.E. Size- and shape-dependent effects of microplastic particles on adult daggerblade grass shrimp (Palaemonetes pugio). Environ. Toxicol. Chem. 2017, 36, 3074–3080. [Google Scholar] [CrossRef]
  68. Villegas, L.; Cabrera, M.; Moulatlet, G.M.; Capparelli, M. The synergistic effect of microplastic and malathion exposure on fiddler crab Minuca ecuadoriensis microplastic bioaccumulation and survival. Mar. Pollut. Bull. 2022, 175, 113336. [Google Scholar] [CrossRef] [PubMed]
  69. Lee, K.; Shim, W.J.; Kwon, O.Y.; Kang, J. Size-dependent effects of micro polystyrene particles in the marine copepod Tigriopus japonicus. Environ. Sci. Technol. 2013, 47, 11278–11283. [Google Scholar] [CrossRef] [PubMed]
  70. Bellas, J.; Gil, I. Polyethylene microplastics increase the toxicity of chlorpyrifos to the marine copepod Acartia tonsa. Environ. Pollut. 2020, 260, 114059. [Google Scholar] [CrossRef]
  71. Syberg, K.; Nielsen, A.; Khan, F.R.; Banta, G.T.; Palmqvist, A.; Jepsen, P.M. Microplastic potentiates triclosan toxicity to the marine copepod Acartia tonsa (Dana). J. Toxicol. Environ. Health Part A 2017, 80, 1369–1371. [Google Scholar] [CrossRef]
  72. Mishra, P.; Vinayagam, S.; Duraisamy, K.; Patil, S.R.; Godbole, J.; Mohan, A.; Mukherjee, A.; Chandrasekaran, N. Distinctive impact of polystyrene nano-spherules as an emergent pollutant toward the environment. Environ. Sci. Pollut. Res. 2019, 26, 1537–1547. [Google Scholar] [CrossRef]
  73. Thiagarajan, V.; Alex, S.A.; Seenivasan, R.; Chandrasekaran, N.; Mukherjee, A. Toxicity evaluation of nano-TiO2 in the presence of functionalized microplastics at two trophic levels: Algae and crustaceans. Sci. Total Environ. 2021, 784, 147262. [Google Scholar] [CrossRef]
  74. Au, S.Y.; Bruce, T.F.; Bridges, W.C.; Klaine, S.J. Responses of Hyalella azteca to acute and chronic microplastic exposures. Environ. Toxicol. Chem. 2015, 34, 2564–2572. [Google Scholar] [CrossRef]
  75. Khan, F.R.; Halle, L.L.; Palmqvist, A. Acute and long-term toxicity of micronized car tire wear particles to Hyalella azteca. Aquat. Toxicol. 2019, 213, 105216. [Google Scholar] [CrossRef] [PubMed]
  76. Yip, Y.J.; Lee, S.S.C.; Neo, M.L.; Teo, S.L.; Valiyaveettil, S. A comparative investigation of toxicity of three polymer nanoparticles on acorn barnacle (Amphibalanus amphitrite). Sci. Total Environ. 2022, 806, 150965. [Google Scholar] [CrossRef]
  77. Schür, C.; Zipp, S.; Thalau, T.; Wagner, M. Microplastics but not natural particles induce multigenerational effects in Daphnia magna. Environ. Pollut. 2020, 260, 113904. [Google Scholar] [CrossRef] [PubMed]
  78. Schür, C.; Weil, C.; Baum, M.; Wallraff, J.; Schreier, M.; Oehlmann, J.; Wagner, M. Incubation in Wastewater Reduces the Multigenerational Effects of Microplastics in Daphnia magna. Environ. Sci. Technol. 2021, 55, 2491–2499. [Google Scholar] [CrossRef]
  79. Eltemsah, Y.S.; Bøhn, T. Acute and chronic effects of polystyrene microplastics on juvenile and adult Daphnia magna. Environ. Pollut. 2019, 254, 112919. [Google Scholar] [CrossRef] [PubMed]
  80. Schwarzer, M.; Brehm, J.; Vollmer, M.; Jasinski, J.; Xu, C.; Zainuddin, S.; Fröhlich, T.; Schott, M.; Greiner, A.; Scheibel, T.; et al. Shape, size, and polymer dependent effects of microplastics on Daphnia magna. J. Hazard. Mater. 2022, 426, 128136. [Google Scholar] [CrossRef]
  81. De Felice, B.; Sabatini, V.; Antenucci, S.; Gattoni, G.; Santo, N.; Bacchetta, R.; Ortenzi, M.A.; Parolini, M. Polystyrene microplastics ingestion induced behavioral effects to the cladoceran Daphnia magna. Chemosphere 2019, 231, 423–431. [Google Scholar] [CrossRef]
  82. Yin, C.; Yang, X.; Zhao, T.; Watson, P.; Yang, F.; Liu, H. Changes of the acute and chronic toxicity of three antimicrobial agents to Daphnia magna in the presence/absence of micro-polystyrene. Environ. Pollut. 2020, 263, 114551. [Google Scholar] [CrossRef] [PubMed]
  83. Pan, Y.; Long, Y.; Hui, J.; Xiao, W.; Yin, J.; Li, Y.; Liu, D.; Tian, Q.; Chen, L. Microplastics can affect the trophic cascade strength and stability of plankton ecosystems via behavior-mediated indirect interactions. J. Hazard. Mater. 2022, 430, 128415. [Google Scholar] [CrossRef]
  84. Liu, Q.; Liu, L.; Huang, J.; Gu, L.; Sun, Y.; Zhang, L.; Lyu, K.; Yang, Z. The response of life history defense of cladocerans under predation risk varies with the size and concentration of microplastics. J. Hazard. Mater. 2022, 427, 127913. [Google Scholar] [CrossRef] [PubMed]
  85. Wang, Z.; Dong, H.; Wang, Y.; Ren, R.; Qin, X.; Wang, S. Effects of microplastics and their adsorption of cadmium as vectors on the cladoceran Moina monogolica Daday: Implications for plastic-ingesting organisms. J. Hazard. Mater. 2020, 400, 123239. [Google Scholar] [CrossRef]
  86. Thi, D.D.; Miranda, A.; Trestrail, C.; De Souza, H.; Dinh, K.V.; Nugegoda, D. Antagonistic effects of copper and microplastics in single and binary mixtures on development and reproduction in the freshwater cladoceran Daphnia carinata. Environ. Technol. Innov. 2021, 24, 102045. [Google Scholar] [CrossRef]
  87. Jaikumar, I.M.; Periyakali, S.B.; Rajendran, U.; Joen-Rong, S.; Thanasekaran, J.; Tsorng-Harn, F. Effects of microplastics, polystyrene, and polyethylene on antioxidants, metabolic enzymes, HSP-70, and myostatin expressions in the giant river prawn Macrobrachium rosenbergii: Impact on survival and growth. Arch. Environ. Contam. Toxicol. 2021, 80, 645–658. [Google Scholar] [CrossRef]
  88. Watts, A.J.R.; Urbina, M.A.; Corr, S.; Lewis, C.; Galloway, T.S. Ingestion of plastic microfibers by the crab Carcinus maenas and its effect on food consumption and energy balance. Environ. Sci. Technol. 2015, 49, 14597–14604. [Google Scholar] [CrossRef]
  89. Jeong, C.; Kang, H.; Lee, M.; Kim, D.; Han, J.; Hwang, D.; Souissi, S.; Lee, S.; Shin, K.; Park, H.G.; et al. Adverse effects of microplastics and oxidative stress-induced MAPK/Nrf2 pathway-mediated defense mechanisms in the marine copepod Paracyclopina nana. Sci. Rep. 2017, 7, 41323. [Google Scholar] [CrossRef] [Green Version]
  90. Jaapar, A.N.; Md Amin, R.; Bhubalan, K.; Sohaimi, E.S. Changes in the development and reproductive output of Nitokra lacustris pacifica (crustacea: Copepoda) yeatman, 1983 under short and long term exposure to synthetic and biodegradable microbeads. J. Polym. Environ. 2021, 29, 4060–4072. [Google Scholar] [CrossRef]
  91. Varó, I.; Perini, A.; Torreblanca, A.; Garcia, Y.; Bergami, E.; Vannuccini, M.L.; Corsi, I. Time-dependent effects of polystyrene nanoparticles in brine shrimp Artemia franciscana at physiological, biochemical and molecular levels. Sci. Total Environ. 2019, 675, 570–580. [Google Scholar] [CrossRef]
  92. Li, H.; Chen, H.; Wang, J.; Li, J.; Liu, S.; Tu, J.; Chen, Y.; Zong, Y.; Zhang, P.; Wang, Z.; et al. Influence of microplastics on the growth and the intestinal microbiota composition of brine shrimp. Front. Microbiol. 2021, 12, 717272. [Google Scholar] [CrossRef] [PubMed]
  93. Redondo-Hasselerharm, P.E.; Falahudin, D.; Peeters, E.T.H.M.; Koelmans, A.A. Microplastic effect thresholds for freshwater benthic macroinvertebrates. Environ. Sci. Technol. 2018, 52, 2278–2286. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  94. Monikh, F.A.; Durão, M.; Kipriianov, P.V.; Huuskonen, H.; Kekäläinen, J.; Uusi-Heikkilä, S.; Uurasjärvi, E.; Akkanen, J.; Kortet, R. Chemical composition and particle size influence the toxicity of nanoscale plastic debris and their co-occurring benzo(α)pyrene in the model aquatic organisms Daphnia magna and Danio rerio. NanoImpact 2022, 25, 100382. [Google Scholar] [CrossRef] [PubMed]
  95. Lee, Y.; Yoon, D.; Lee, Y.H.; Kwak, J.I.; An, Y.; Lee, J.; Park, J.C. Combined exposure to microplastics and zinc produces sex-specific responses in the water flea Daphnia magna. J. Hazard. Mater. 2021, 420, 126652. [Google Scholar] [CrossRef]
  96. Ogonowski, M.; Schür, C.; Jarsén, Å.; Gorokhova, E. The effects of natural and anthropogenic microparticles on individual fitness in Daphnia magna. PLoS ONE 2016, 11, e155063. [Google Scholar] [CrossRef] [Green Version]
  97. Zimmermann, L.; Göttlich, S.; Oehlmann, J.; Wagner, M.; Völker, C. What are the drivers of microplastic toxicity? Comparing the toxicity of plastic chemicals and particles to Daphnia magna. Environ. Pollut. 2020, 267, 115392. [Google Scholar] [CrossRef]
  98. Jaikumar, G.; Brun, N.R.; Vijver, M.G.; Bosker, T. Reproductive toxicity of primary and secondary microplastics to three cladocerans during chronic exposure. Environ. Pollut. 2019, 249, 638–646. [Google Scholar] [CrossRef] [Green Version]
  99. Zhang, C.; Jeong, C.; Lee, J.; Wang, D.; Wang, M. Transgenerational proteome plasticity in resilience of a marine copepod in response to environmentally relevant concentrations of microplastics. Environ. Sci. Technol. 2019, 53, 8426–8436. [Google Scholar] [CrossRef]
  100. Li, Z.; Zhou, H.; Liu, Y.; Zhan, J.; Li, W.; Yang, K.; Yi, X. Acute and chronic combined effect of polystyrene microplastics and dibutyl phthalate on the marine copepod Tigriopus japonicus. Chemosphere 2020, 261, 127711. [Google Scholar] [CrossRef]
  101. Rodríguez-Torres, R.; Almeda, R.; Kristiansen, M.; Rist, S.; Winding, M.S.; Nielsen, T.G. Ingestion and impact of microplastics on arctic Calanus copepods. Aquat. Toxicol. 2020, 228, 105631. [Google Scholar] [CrossRef]
  102. Heindler, F.M.; Alajmi, F.; Huerlimann, R.; Zeng, C.; Newman, S.J.; Vamvounis, G.; van Herwerden, L. Toxic effects of polyethylene terephthalate microparticles and Di(2-ethylhexyl)phthalate on the calanoid copepod, Parvocalanus crassirostris. Ecotoxicol. Environ. Saf. 2017, 141, 298–305. [Google Scholar] [CrossRef]
  103. Peixoto, D.; Amorim, J.; Pinheiro, C.; Oliva-Teles, L.; Varó, I.; de Medeiros Rocha, R.; Vieira, M.N. Uptake and effects of different concentrations of spherical polymer microparticles on Artemia franciscana. Ecotoxicol. Environ. Saf. 2019, 176, 211–218. [Google Scholar] [CrossRef] [PubMed]
  104. Cheng, Y.; Wang, J.; Yi, X.; Li, L.; Liu, X.; Ru, S. Low microalgae availability increases the ingestion rates and potential effects of microplastics on marine copepod Pseudodiaptomus annandalei. Mar. Pollut. Bull. 2020, 152, 110919. [Google Scholar] [CrossRef] [PubMed]
  105. Coppock, R.L.; Galloway, T.S.; Cole, M.; Fileman, E.S.; Queirós, A.M.; Lindeque, P.K. Microplastics alter feeding selectivity and faecal density in the copepod, Calanus helgolandicus. Sci. Total Environ. 2019, 687, 780–789. [Google Scholar] [CrossRef] [PubMed]
  106. Cole, M.; Coppock, R.; Lindeque, P.K.; Altin, D.; Reed, S.; Pond, D.W.; Sørensen, L.; Galloway, T.S.; Booth, A.M. Effects of nylon microplastic on feeding, lipid accumulation, and moulting in a coldwater copepod. Environ. Sci. Technol. 2019, 53, 7075–7082. [Google Scholar] [CrossRef] [Green Version]
  107. Almeda, R.; Rodriguez-Torres, R.; Rist, S.; Winding, M.H.S.; Stief, P.; Hansen, B.H.; Nielsen, T.G. Microplastics do not increase bioaccumulation of petroleum hydrocarbons in Arctic zooplankton but trigger feeding suppression under co-exposure conditions. Sci. Total Environ. 2021, 751, 141264. [Google Scholar] [CrossRef] [PubMed]
  108. Colomer, J.; Müller, M.F.; Barcelona, A.; Serra, T. Mediated food and hydrodynamics on the ingestion of microplastics by Daphnia magna. Environ. Pollut. 2019, 251, 434–441. [Google Scholar] [CrossRef]
  109. Serra, T.; Barcelona, A.; Pous, N.; Salvadó, V.; Colomer, J. Synergistic effects of water temperature, microplastics and ammonium as second and third order stressors on Daphnia magna. Environ. Pollut. 2020, 267, 115439. [Google Scholar] [CrossRef]
  110. Chen, Q.; Li, Y.; Li, B. Is color a matter of concern during microplastic exposure to Scenedesmus obliquus and Daphnia magna? J. Hazard. Mater. 2020, 383, 121224. [Google Scholar] [CrossRef]
  111. Kim, D.; Kim, H.; An, Y. Effects of synthetic and natural microfibers on Daphnia magna–Are they dependent on microfiber type? Aquat. Toxicol. 2021, 240, 105968. [Google Scholar] [CrossRef]
  112. Wang, Y.; Mao, Z.; Zhang, M.; Ding, G.; Sun, J.; Du, M.; Liu, Q.; Cong, Y.; Jin, F.; Zhang, W.; et al. The uptake and elimination of polystyrene microplastics by the brine shrimp, Artemia parthenogenetica, and its impact on its feeding behavior and intestinal histology. Chemosphere 2019, 234, 123–131. [Google Scholar] [CrossRef]
  113. Pikuda, O.; Xu, E.G.; Berk, D.; Tufenkji, N. Toxicity assessments of micro- and nanoplastics can be confounded by preservatives in commercial formulations. Environ. Sci. Technol. Lett. 2019, 6, 21–25. [Google Scholar] [CrossRef]
  114. Song, J.; Na, J.; An, D.; Jung, J. Role of benzophenone-3 additive in chronic toxicity of polyethylene microplastic fragments to Daphnia magna. Sci. Total Environ. 2021, 800, 149638. [Google Scholar] [CrossRef] [PubMed]
  115. Bartonitz, A.; Anyanwu, I.N.; Geist, J.; Imhof, H.K.; Reichel, J.; Graßmann, J.; Drewes, J.E.; Beggel, S. Modulation of PAH toxicity on the freshwater organism G. roeseli by microparticles. Environ. Pollut. 2020, 260, 113999. [Google Scholar] [CrossRef] [PubMed]
  116. Gambardella, C.; Morgana, S.; Ferrando, S.; Bramini, M.; Piazza, V.; Costa, E.; Garaventa, F.; Faimali, M. Effects of polystyrene microbeads in marine planktonic crustaceans. Ecotoxicol. Environ. Saf. 2017, 145, 250–257. [Google Scholar] [CrossRef]
  117. Procter, J.; Hopkins, F.E.; Fileman, E.S.; Lindeque, P.K. Smells good enough to eat: Dimethyl sulfide (DMS) enhances copepod ingestion of microplastics. Mar. Pollut. Bull. 2019, 138, 1–6. [Google Scholar] [CrossRef]
  118. Cunningham, E.M.; Mundye, A.; Kregting, L.; Dick, J.T.A.; Crump, A.; Riddell, G.; Arnott, G. Animal contests and microplastics: Evidence of disrupted behaviour in hermit crabs Pagurus bernhardus. R. Soc. Open Sci. 2021, 8, 211089. [Google Scholar] [CrossRef]
  119. Yu, P.; Liu, Z.; Wu, D.; Chen, M.; Lv, W.; Zhao, Y. Accumulation of polystyrene microplastics in juvenile Eriocheir sinensis and oxidative stress effects in the liver. Aquat. Toxicol. 2018, 200, 28–36. [Google Scholar] [CrossRef]
  120. Liu, Z.; Li, Y.; Sepúlveda, M.S.; Jiang, Q.; Jiao, Y.; Chen, Q.; Huang, Y.; Tian, J.; Zhao, Y. Development of an adverse outcome pathway for nanoplastic toxicity in Daphnia pulex using proteomics. Sci. Total Environ. 2021, 766, 144249. [Google Scholar] [CrossRef]
  121. Abdolahpur Monikh, F.; Vijver, M.G.; Guo, Z.; Zhang, P.; Darbha, G.K.; Peijnenburg, W.J.G.M. Metal sorption onto nanoscale plastic debris and trojan horse effects in Daphnia magna: Role of dissolved organic matter. Water Res. 2020, 186, 116410. [Google Scholar] [CrossRef]
  122. Yoo, J.; Cho, H.; Jeon, M.; Jeong, C.; Jung, J.; Lee, Y. Effects of polystyrene in the brackish water flea Diaphanosoma celebensis: Size-dependent acute toxicity, ingestion, egestion, and antioxidant response. Aquat. Toxicol. 2021, 235, 105821. [Google Scholar] [CrossRef] [PubMed]
  123. Zhang, F.; Wang, Z.; Wang, S.; Fang, H.; Wang, D. Aquatic behavior and toxicity of polystyrene nanoplastic particles with different functional groups: Complex roles of pH, dissolved organic carbon and divalent cations. Chemosphere 2019, 228, 195–203. [Google Scholar] [CrossRef] [PubMed]
  124. Suman, T.Y.; Jia, P.; Li, W.; Junaid, M.; Xin, G.; Wang, Y.; Pei, D. Acute and chronic effects of polystyrene microplastics on brine shrimp: First evidence highlighting the molecular mechanism through transcriptome analysis. J. Hazard. Mater. 2020, 400, 123220. [Google Scholar] [CrossRef] [PubMed]
  125. Eom, H.; Haque, M.N.; Lee, S.; Rhee, J. Exposure to metals premixed with microplastics increases toxicity through bioconcentration and impairs antioxidant defense and cholinergic response in a marine mysid. Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 2021, 249, 109142. [Google Scholar] [CrossRef] [PubMed]
  126. Peixoto, D.; Torreblanca, A.; Pereira, S.; Vieira, M.N.; Varó, I. Effect of short-term exposure to fluorescent red polymer microspheres on Artemia franciscana nauplii and juveniles. Environ. Sci. Pollut. Res. 2022, 29, 6080–6092. [Google Scholar] [CrossRef]
  127. Kim, J.; Rhee, J. Biochemical and physiological responses of the water flea Moina macrocopa to microplastics: A multigenerational study. Mol. Cell. Toxicol. 2021, 17, 523–532. [Google Scholar] [CrossRef]
  128. Hoffschröer, N.; Grassl, N.; Steinmetz, A.; Sziegoleit, L.; Koch, M.; Zeis, B. Microplastic burden in Daphnia is aggravated by elevated temperatures. Zoology 2021, 144, 125881. [Google Scholar] [CrossRef]
  129. Hiltunen, M.; Vehniäinen, E.; Kukkonen, J.V.K. Interacting effects of simulated eutrophication, temperature increase, and microplastic exposure on Daphnia. Environ. Res. 2021, 192, 110304. [Google Scholar] [CrossRef]
  130. Chae, Y.; Kim, D.; Choi, M.; Cho, Y.; An, Y. Impact of nano-sized plastic on the nutritional value and gut microbiota of whiteleg shrimp Litopenaeus vannamei via dietary exposure. Environ. Int. 2019, 130, 104848. [Google Scholar] [CrossRef]
  131. Cole, M.; Lindeque, P.; Fileman, E.; Halsband, C.; Galloway, T.S. The impact of polystyrene microplastics on feeding, function and fecundity in the marine copepod Calanus helgolandicus. Environ. Sci. Technol. 2015, 49, 1130–1137. [Google Scholar] [CrossRef]
  132. Welden, N.A.C.; Cowie, P.R. Long-term microplastic retention causes reduced body condition in the langoustine, Nephrops norvegicus. Environ. Pollut. 2016, 218, 895–900. [Google Scholar] [CrossRef] [Green Version]
  133. Tourinho, P.S.; Silva, A.R.R.; Santos, C.S.A.; Prodana, M.; Ferreira, V.; Habibullah, G.; Kočí, V.; Gestel, C.A.M.; Loureiro, S. Microplastic fibers increase sublethal effects of AgNP and AgNO3 in Daphnia magna by changing cellular energy allocation. Environ. Toxicol. Chem. 2022, 41, 896–904. [Google Scholar] [CrossRef]
  134. Duan, Y.; Xiong, D.; Wang, Y.; Zhang, Z.; Li, H.; Dong, H.; Zhang, J. Toxicological effects of microplastics in Litopenaeus vannamei as indicated by an integrated microbiome, proteomic and metabolomic approach. Sci. Total Environ. 2021, 761, 143311. [Google Scholar] [CrossRef] [PubMed]
  135. Korez, Š.; Gutow, L.; Saborowski, R. Feeding and digestion of the marine isopod Idotea emarginata challenged by poor food quality and microplastics. Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 2019, 226, 108586. [Google Scholar] [CrossRef] [PubMed]
  136. Chen, Q.; Lv, W.; Jiao, Y.; Liu, Z.; Li, Y.; Cai, M.; Wu, D.; Zhou, W.; Zhao, Y. Effects of exposure to waterborne polystyrene microspheres on lipid metabolism in the hepatopancreas of juvenile redclaw crayfish, Cherax quadricarinatus. Aquat. Toxicol. 2020, 224, 105497. [Google Scholar] [CrossRef]
  137. Han, Y.; Shi, W.; Tang, Y.; Zhou, W.; Sun, H.; Zhang, J.; Yan, M.; Hu, L.; Liu, G. Microplastics and bisphenol A hamper gonadal development of whiteleg shrimp (Litopenaeus vannamei) by interfering with metabolism and disrupting hormone regulation. Sci. Total Environ. 2022, 810, 152354. [Google Scholar] [CrossRef]
  138. Svetlichny, L.; Isinibilir, M.; Mykitchak, T.; Eryalçın, K.M.; Türkeri, E.E.; Yuksel, E.; Kideys, A.E. Microplastic consumption and physiological response in Acartia clausi and Centropages typicus: Possible roles of feeding mechanisms. Reg. Stud. Mar. Sci. 2021, 43, 101650. [Google Scholar] [CrossRef]
  139. Isinibilir, M.; Svetlichny, L.; Mykitchak, T.; Türkeri, E.E.; Eryalçın, K.M.; Doğan, O.; Can, G.; Yüksel, E.; Kideys, A.E. Microplastic consumption and its effect on respiration rate and motility of Calanus helgolandicus from the marmara sea. Front. Mar. Sci. 2020, 7, 603321. [Google Scholar] [CrossRef]
  140. Woods, M.N.; Hong, T.J.; Baughman, D.; Andrews, G.; Fields, D.M.; Matrai, P.A. Accumulation and effects of microplastic fibers in American lobster larvae (Homarus americanus). Mar. Pollut. Bull. 2020, 157, 111280. [Google Scholar] [CrossRef]
  141. Watts, A.J.R.; Urbina, M.A.; Goodhead, R.; Moger, J.; Lewis, C.; Galloway, T.S. Effect of microplastic on the gills of the shore crab Carcinus maenas. Environ. Sci. Technol. 2016, 50, 5364–5369. [Google Scholar] [CrossRef] [Green Version]
  142. Kratina, P.; Watts, T.J.; Green, D.S.; Kordas, R.L.; O’Gorman, E.J. Interactive effects of warming and microplastics on metabolism but not feeding rates of a key freshwater detritivore. Environ. Pollut. 2019, 255, 113259. [Google Scholar] [CrossRef]
  143. Sadler, D.E.; Brunner, F.S.; Plaistow, S.J. Temperature and clone-dependent effects of microplastics on immunity and life history in Daphnia magna. Environ. Pollut. 2019, 255, 113178. [Google Scholar] [CrossRef]
  144. Liu, Z.; Yu, P.; Cai, M.; Wu, D.; Zhang, M.; Chen, M.; Zhao, Y. Effects of microplastics on the innate immunity and intestinal microflora of juvenile Eriocheir sinensis. Sci. Total Environ. 2019, 685, 836–846. [Google Scholar] [CrossRef]
  145. Liu, Z.; Li, Y.; Pérez, E.; Jiang, Q.; Chen, Q.; Jiao, Y.; Huang, Y.; Yang, Y.; Zhao, Y. Polystyrene nanoplastic induces oxidative stress, immune defense, and glycometabolism change in Daphnia pulex: Application of transcriptome profiling in risk assessment of nanoplastics. J. Hazard. Mater. 2021, 402, 123778. [Google Scholar] [CrossRef] [PubMed]
  146. Liu, Z.; Huang, Y.; Jiao, Y.; Chen, Q.; Wu, D.; Yu, P.; Li, Y.; Cai, M.; Zhao, Y. Polystyrene nanoplastic induces ROS production and affects the MAPK-HIF-1/NFkB-mediated antioxidant system in Daphnia pulex. Aquat. Toxicol. 2020, 220, 105420. [Google Scholar] [CrossRef]
  147. Liu, Z.; Cai, M.; Wu, D.; Yu, P.; Jiao, Y.; Jiang, Q.; Zhao, Y. Effects of nanoplastics at predicted environmental concentration on Daphnia pulex after exposure through multiple generations. Environ. Pollut. 2020, 256, 113506. [Google Scholar] [CrossRef] [PubMed]
  148. Liu, Z.; Cai, M.; Yu, P.; Chen, M.; Wu, D.; Zhang, M.; Zhao, Y. Age-dependent survival, stress defense, and AMPK in Daphnia pulex after short-term exposure to a polystyrene nanoplastic. Aquat. Toxicol. 2018, 204, 1–8. [Google Scholar] [CrossRef] [PubMed]
  149. Li, Y.; Liu, Z.; Jiang, Q.; Ye, Y.; Zhao, Y. Effects of nanoplastic on cell apoptosis and ion regulation in the gills of Macrobrachium nipponense. Environ. Pollut. 2022, 300, 118989. [Google Scholar] [CrossRef]
  150. Trotter, B.; Wilde, M.V.; Brehm, J.; Dafni, E.; Aliu, A.; Arnold, G.J.; Fröhlich, T.; Laforsch, C. Long-term exposure of Daphnia magna to polystyrene microplastic (PS-MP) leads to alterations of the proteome, morphology and life-history. Sci. Total Environ. 2021, 795, 148822. [Google Scholar] [CrossRef]
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Figure 1. Effects of microplastics on aquatic crustaceans.
Figure 1. Effects of microplastics on aquatic crustaceans.
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Figure 2. The number of papers on the effects of microplastics on the life history, behavior and physiological function of aquatic crustacean. The number of papers examining the life history, behavior and physiological function of aquatic crustacean impacted by microplastics are shown in (A,C,E), respectively. The number of papers on aquatic species involved in the life history, behavior and physiological function of aquatic crustacean are shown in (B,D,F), respectively.
Figure 2. The number of papers on the effects of microplastics on the life history, behavior and physiological function of aquatic crustacean. The number of papers examining the life history, behavior and physiological function of aquatic crustacean impacted by microplastics are shown in (A,C,E), respectively. The number of papers on aquatic species involved in the life history, behavior and physiological function of aquatic crustacean are shown in (B,D,F), respectively.
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Zhang, S.; Wu, H.; Hou, J. Progress on the Effects of Microplastics on Aquatic Crustaceans: A Review. Int. J. Mol. Sci. 2023, 24, 5523. https://doi.org/10.3390/ijms24065523

AMA Style

Zhang S, Wu H, Hou J. Progress on the Effects of Microplastics on Aquatic Crustaceans: A Review. International Journal of Molecular Sciences. 2023; 24(6):5523. https://doi.org/10.3390/ijms24065523

Chicago/Turabian Style

Zhang, Siyi, Haodi Wu, and Jing Hou. 2023. "Progress on the Effects of Microplastics on Aquatic Crustaceans: A Review" International Journal of Molecular Sciences 24, no. 6: 5523. https://doi.org/10.3390/ijms24065523

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