ACS Publications. Most Trusted. Most Cited. Most Read
My Activity
CONTENT TYPES

Figure 1Loading Img

Effects of Nylon Microplastic on Feeding, Lipid Accumulation, and Moulting in a Coldwater Copepod

  • Matthew Cole*
    Matthew Cole
    Marine Ecology and Biodiversity Group, Plymouth Marine Laboratory, Plymouth PL1 3DH, United Kingdom
    *Phone: +44(0)1752 633100; e-mail: [email protected]
    More by Matthew Cole
  • Rachel Coppock
    Rachel Coppock
    Marine Ecology and Biodiversity Group, Plymouth Marine Laboratory, Plymouth PL1 3DH, United Kingdom
    College of Life and Environmental Sciences: Biosciences, University of Exeter, Exeter EX4 4QD, United Kingdom
  • Penelope K. Lindeque*
    Penelope K. Lindeque
    Marine Ecology and Biodiversity Group, Plymouth Marine Laboratory, Plymouth PL1 3DH, United Kingdom
    *Phone: +44(0)1752 633100; e-mail: [email protected]
  • Dag Altin
    Dag Altin
    BioTrix, Trondheim NO-7022, Norway
    More by Dag Altin
  • Sarah Reed
    Sarah Reed
    Scottish Association of Marine Science, Scottish Marine Institute, Oban PA37 1QA, United Kingdom
    More by Sarah Reed
  • David W. Pond
    David W. Pond
    Scottish Association of Marine Science, Scottish Marine Institute, Oban PA37 1QA, United Kingdom
    Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, United Kingdom
  • Lisbet Sørensen
    Lisbet Sørensen
    SINTEF Ocean AS, Trondheim NO-7465, Norway
  • Tamara S. Galloway
    Tamara S. Galloway
    College of Life and Environmental Sciences: Biosciences, University of Exeter, Exeter EX4 4QD, United Kingdom
  • , and 
  • Andy M. Booth
    Andy M. Booth
    SINTEF Ocean AS, Trondheim NO-7465, Norway
Cite this: Environ. Sci. Technol. 2019, 53, 12, 7075–7082
Publication Date (Web):May 24, 2019
https://doi.org/10.1021/acs.est.9b01853

Copyright © 2022 American Chemical Society. This publication is licensed under CC-BY.

  • Open Access

Article Views

10923

Altmetric

-

Citations

LEARN ABOUT THESE METRICS
PDF (2 MB)
Supporting Info (1)»

Abstract

Microplastic debris is a pervasive environmental contaminant that has the potential to impact the health of biota, although its modes of action remain somewhat unclear. The current study tested the hypothesis that exposure to fibrous and particulate microplastics would alter feeding, impacting on lipid accumulation, and normal development (e.g., growth, moulting) in an ecologically important coldwater copepod Calanus finmarchicus. Preadult copepods were incubated in seawater containing a mixed assemblage of cultured microalgae (control), with the addition of ∼50 microplastics mL–1 of nylon microplastic granules (10–30 μm) or fibers (10 × 30 μm), which are similar in shape and size to the microalgal prey. The additive chemical profiles showed the presence of stabilizers, lubricants, monomer residues, and byproducts. Prey selectivity was significantly altered in copepods exposed to nylon fibers (ANOVA, P < 0.01) resulting in a nonsignificant 40% decrease in algal ingestion rates (ANOVA, P = 0.07), and copepods exposed to nylon granules showed nonsignificant lipid accumulation (ANOVA, P = 0.62). Both microplastics triggered premature moulting in juvenile copepods (Bernoulli GLM, P < 0.01). Our results emphasize that the shape and chemical profile of a microplastic can influence its bioavailability and toxicity, drawing attention to the importance of using environmentally relevant microplastics and chemically profiling plastics used in toxicity testing.

Introduction

ARTICLE SECTIONS
Jump To

Microplastics (1 μm to 1 mm) are a pervasive and persistent environmental contaminant, impinging on freshwater, terrestrial, and marine ecosystems across the globe. (1,2) These synthetic particulates and fibers are either directly manufactured (e.g., exfoliates in personal care products), or derive from fragmentation of larger plastic debris. (3,4) It is conservatively estimated that over 4.75 × 1012 plastic particles (in the size range of 0.3–4.5 mm) are floating in the global ocean. (5) As complete mineralization of plastic debris is estimated to range from tens to hundreds of years, and with plastic inputs expected to rise for the foreseeable future, marine microplastic concentrations are likely to increase. (6,7) Owing to their small size, microplastics can be directly or indirectly (i.e., via trophic interactions) ingested by a range of marine organisms across trophic levels, including zooplankton, (8) shellfish, (9) fish, (10,11) and megafauna. (12,13) Microplastics contain additives, plasticizers, and monomers (e.g., bisphenol A, polybrominated diphenyl ethers) incorporated during their manufacture to provide a wide range of functions including as emollients, stabilizers, and flame retardants. (14) Furthermore, they may carry persistent organic pollutants (POPs), metals, and pathogens that adsorb or adhere to their surface in the marine environment. (15,16) Where equilibrium has not been reached (i.e., there is a chemical gradient), there is evidence that POPs and metals (e.g., copper, zinc) can transfer from microplastics into biota potentially enhancing their toxicity. (17,18) Laboratory testing has highlighted the negative impacts microplastic ingestion can have on marine organisms, including zooplankton, mussels, oysters, crustaceans, and fish, with effects including reduced feeding, fecundity, growth, and survival. (19−24) These effects can cascade through levels of biological organization, resulting in impacts on the ecological functionality of keystone species (e.g., bioturbation, nutrient cycling). (25)
Copepods are an abundant class of marine zooplankton that provide an essential trophic link between primary producers and secondary consumers, and contribute to ecological processes such as marine nutrient cycling. (26) Laboratory exposures have demonstrated the capacity for a range of pelagic and benthic copepods, including Acartia spp., Calanus spp, Centropages spp., Limnocalanus spp., Temora spp., and Tigriopus spp., to ingest polystyrene microplastic beads and fragments. (27−30) Furthermore, wild copepods sampled from the South China Sea (31) and Northeast Pacific Ocean (32) have been shown to ingest microplastic fibers and particulates in the natural environment. Exposure studies have highlighted that polystyrene microspheres can negatively affect copepod feeding and health. Exposed to a monoalgal diet and polystyrene beads (20 μm; 65 microplastics mL–1), the temperate calanoid copepod Calanus helgolandicus showed significant reductions in their dietary intake of carbon owing to a shift in feeding, with a preference for smaller, less nutritious algae. (22) After 3 days exposure, Cole et al. (22) observed microplastic exposed copepods produced significantly smaller eggs with reduced hatching success, which was attributed to reduced energetic intake. There is relatively little data currently available to determine whether microplastics with different physical properties (e.g., shape, size, density) (33) will exhibit altered bioavailability or toxicity, and there are few published microplastic exposure studies focused on early life stages. Incorporation of microplastics more representative of those found in the environment (i.e., irregularly shaped, fibers) and consideration of impacts on early life stages have been encouraged within the scientific community. (34,35)
In this study, we investigate the impact of fibrous and particulate microplastic exposure on feeding, lipid accumulation, growth, and moulting in preadult Calanus finmarchicus, a boreal (coldwater) copepod that is widely distributed in the northern hemisphere and the dominant mesozooplankton species in the North Sea and Norwegian Sea. (36) The energetic reserve of C. finmarchicus takes the form of a large oil sac, comprising wax esters with long-chain fatty acids and fatty alcohols, built-up during their juvenile life stages in periods of high food availability. (37,38) These lipid stores make C. finmarchicus nutritionally valuable to higher-trophic organisms (e.g., fish, whales), and facilitate “diapause”, whereby the copepods descend to deeper waters and enter a state of dormancy over winter. (39,40) We hypothesized that reductions in algal feeding stemming from microplastic exposure would result in reduced lipid accumulation in developing C. finmarchicus with consequences for the normal development of the copepod. In our experiments, cohorts of preadult C. finmarchicus (copepodite stage, CV) were exposed to mixed algal assemblages with the addition of either nylon microplastic fibers or granules at a concentration of 50 microplastics mL–1 for 6 days, with sublethal end points including: algal ingestion rates, growth, lipid mass and profiles, and moulting. Our results provide evidence of the risks fibrous and particulate microplastics pose to the energetics and development of a keystone species.

Materials and Methods

ARTICLE SECTIONS
Jump To

Copepods and Microalgae

Juvenile Calanus finmarchicus (CV) were subsampled from copepod cultures maintained at the Norwegian University of Science and Technology (NTNU). Copepods were fed a mixed assemblage of three microalgal species of different size and shape (Supporting Information, SI, Figure S1), which are part of the natural diet of Calanus sp.: (i) the chlorophyte Dunaliella tertiolecta (9 × 13 μm); (ii) the chain-forming diatom Thalassiosira rotula (19 × 24 μm); and (iii) the dinoflagellate Scripsiella trochoidea (29 × 34 μm). Algae were cultured with F/2 media, with addition of silica for T. rotula, and maintained at 18 °C at a 16:8 light/dark cycle. Copepods were fed a nonlimiting concentration of microalgae, comprising ∼200 cells mL–1 of D. tertiolecta, ∼50 cell mL–1 of T. rotula, and ∼15 cells mL–1 of S. trochoidea. D. tertiolecta were quantified using a Coulter Counter (Beckman Multisizer 3), while T. rotula and S. trochoidea were quantified using a Sedgewick rafter chamber. C. finmarchicus were acclimated to their algal prey for 48 h prior to experiments. The carbon biomass of algal prey was estimated using a literature derived conversion factor of 5 nL biovolume ≈ 1 μg C. (41) To calculate algal biovolume, microalgae were imaged under an inverted microscope (Nikon TE2000S), cellular dimensions determined using ImageJ, and the formulas for a volume of an ellipsoid (D. tertiolecta and S. trochoidea) or cylinder (T. rotula) applied.

Microplastics

Nylon fibers (10 × 30 μm), of a similar shape and size as the chain-forming microalgae T. rotula, were prepared by sectioning polyamide nylon-6,6 polyfilament line (Goodfellow; AM325705) per the method of Cole (2016). (42) In brief, the polyfilament line was wrapped continuously around a custom spool, embedded in TissueTek cryogenic solution, and then sectioned at 30 μm intervals using a cryogenic microtome (LEICA CM1950). Nylon granules (10–30 μm), of a similar shape and size distribution as the unicellular microalgae D. tertiolecta and S. trochoidea, were prepared by size fractionating polyamide nylon-6 powder (Goodfellow; AM306010) with 30 μm nylon mesh and 10 μm polycarbonate membrane filters. Prior to use, microplastics were rinsed with ethanol and copious amounts of ultrapure water, suspended in ultrapure water and quantified using a Sedgewick rafter chamber. For imaging purposes, a subsample of the fibrous and granular microplastics were dyed with Nile Red (500 μg mL–1).

Chemical Profiling

To ascertain what compounds (e.g., monomers, additives) were present in the microplastics, samples of fibers (∼20 mg) and granules (∼50 mg) were extracted using either 4 mL of dichloromethane (DCM, Rathburn; n = 3) or 4 mL of ethyl acetate (EtOAc, Fluka; n = 3). Solvent was added to each sample and then the sample sonicated for 30 min (Bandelin Sonorex Super RK 510H ultrasonication bath, 640W, 35 kHz) at either room temperature (DCM) or 65 °C (EtOAc). The solvent extract was filtered through a pipette packed with Bilson cotton and a small amount (∼50 mg) of anhydrous Na2SO4 to remove particulates, and then concentrated by solvent evaporation (40 °C under a gentle flow of N2) to an approximate volume of 500 μL prior to analysis by GC-MS (Agilent 7890A GC equipped with an Agilent 5975C Mass Selective Detector). Here, the inlet was set to 250 °C, the transfer line to 300 °C, the ion source to 230 °C and the quadrupole to 150 °C. The carrier gas was helium, at a constant flow of 1.1 mL/min. One μL of sample was injected by pulsed splitless injection (Agilent DB5-MS ultrainert GC column; 30 m, 0.25 μm film thickness, 0.25 mm internal diameter). The GC oven was held at 40 °C (2 min), ramped by 6 °C min–1 to 320 °C (20 min hold). Mass spectra were recorded after 12 min of hold time (50–500 m/z). Chromatograms and mass spectra were recorded using Chemstation software, investigated in Masshunter Qualitative Navigator B.08.00, further processed using Masshunter Unknowns Analysis (“Unknowns”) followed by export to csv format using Python and data processed in R. After initial inspection of chromatograms, peaks were deconvoluted using Unknowns algorithms and best hits from the NIST 2017 library were extracted. Compounds were filtered based on observed presence in at least 3 of the 6 total replicates and >80% match to NIST 2017 library mass spectra.

Exposure

Treatments comprised: (i) controls, (ii) nylon fibers, and (iii) nylon granules. Exposure media consisted of 0.22 μm filtered natural seawater containing mixed algal prey and 20 mL of Guillard’s F/2 media to ensure water remained nutrient replete, plus 50 microplastics mL–1 of nylon fibers or granules as applicable. Stocks were prepared daily, thoroughly mixed with a perforated plunger, and then carefully poured into 1 L glass bottles (n = 10 per treatment). Ten preadult copepods (copepodite stage CV) were added to each bottle, and exposure media used to fill all bottles to the brim (total volume 1150 mL), thereby eliminating air bubbles. To account for the natural growth of the algae (see Algal ingestion rates), exposure media in 500 mL bottles (n = 5) was also incubated without copepods on Day 3–4. Bottles were secured to a rotating plankton wheel (<5 rpm) submerged in a water bath for temperature stability, and the setup maintained at 8.7 ± 0.1 °C in the dark for a total of 6 days. Water changes were conducted daily by gently pouring the contents of each bottle through a partially submerged 500 μm mesh to isolate copepods; on Day 3–4 media was preserved for calculation of algal ingestion rates. The developmental stage of each copepod was noted (see Moulting), and then the specimens transferred to fresh media. Any individuals damaged during water changes were removed and if experimental cohorts were reduced by >50% the replicate was rejected. At the end of the exposure, copepods were anaesthetised using FinQuel (MS222), and then photographed under a stereo microscope (Leica MZAPO/Nikon DigitalSight Fi1-U2). Individual copepods were transferred to a cryovial, snap-frozen in liquid nitrogen and subsequently stored at −80 °C prior to lipid analysis.

Microplastic Uptake

To verify that juvenile C. finmarchicus had the capacity to ingest microplastics, we conducted a 2 h exposure (per the experimental protocol described above) using nylon fibers and granules dyed with Nile Red (100 microplastics mL–1). Following the exposure, copepods and their faecal pellets were isolated using a 63 μm mesh, transferred to a clean glass Petri dish, and subsequently visualized and photographed under a stereo microscope (Leica MZAPO/Nikon DigitalSight Fi1-U2) equipped with a stereofluorescence module (Leica “green” fluorescent filter; excitation 546/10 nm, dichroic splitter 565 nm and emission OG590).

Algal Ingestion Rates

Feeding rates (i.e., algal ingestion rates) were assessed midway through the exposure (Day 3–4). At T0 (Day 3), 200 mL subsamples of algal stocks were collected and preserved with 2% Lugols solution (n = 5 per treatment). After 24 h (Day 4), 200 mL subsamples were taken from all bottles (including algal controls without predation), and fixed with 2% Lugols. Preserved samples were maintained in amber glass bottles prior to analysis to prevent degradation. Microalgae were quantified using the Utermöhl technique (BSEN15204:2006). In brief, samples were settled in 100 mL Utermöhl chambers for 48 h, samples viewed under inverted microscope (Olympus IMT2) and cells systematically enumerated. Cell concentrations and mean carbon biomass of the microalgae were subsequently used to calculate algal ingestion rates (μg C individual–1 day–1) per the equation of Frost. (43)

Prosome Length

The prosome length (μm) of copepods was ascertained for copepods subsampled from initial stocks (Day 0, n = 25) and juvenile, female and male copepods at the end of the 6-day exposure. In all cases, individual copepods were anaesthetised and photographed under a stereo microscope (Leica MZAPO/Nikon DigitalSight Fi1-U2), and prosome length measured using ImageJ software.

Total Lipid Mass and Lipid Profiles

Copepod lipids were extracted by adapting the protocol of Folch et al., (44) adding 500 μL of chloroform–methanol (2:1 v/v) and then placing the sample in a −20 °C freezer for 4 h. Next, a phase separation of nonpolar lipids and polar organics/compounds was undertaken by adding 130 μL potassium chloride (0.88% w/w), and then vortexing (12–16 rpm), and centrifuging (2.5 min, 2500 rpm) the sample. A glass-steel pipette was used to carefully extract and transfer the bottom phase (containing nonpolar lipids) to a preweighed glass vial. The solvent was gently evaporated using nitrogen gas, and the sample desiccated under vacuum in the dark for 30 min. Finally, the vial was weighed on a mass balance to ascertain the total lipid mass (mg). To assess the lipid content of the microalgae, 1–2 mL of microalgae were filtered through a GFF; filters were placed in 7 mL glass vials, the lipids extracted using 5 mL of chloroform–methanol (2:1 v/v), and then processed as above. Prior to lipid profiling, 250 μL of chloroform was added to each vial, and samples stored at −20 °C. For determination of lipid profiles, internal standards (23:0, fatty acid and 19:0 fatty alcohol) were added to the total lipid samples prior to methylation in 1% methanol for 16 h at 50 °C. Fatty acid methyl esters and free fatty alcohols were purified using High Performance Thin Layer Chromatography (HPTLC) and analyzed by gas chromatography using a Thermo Trace 2000 GC equipped with a Resteck Stabilwax column.

Moulting

Every 24 h the developmental stage of copepods was determined, based upon the morphological characteristics of each copepod (SI Figure S2). For adult copepods, their sex was determined at the end of the exposure period through morphological assessment of anaesthetised specimens.

Statistical Analyses

Statistical analysis was conducted using R statistical software V 1.0.136. (45) Data were tested for normality using a Shapiro-Wilk test and homogeneity of variance was visually inspected to satisfy apriori parametric requisites. An ANOVA with posthoc Tukey tests was used to compare biological data including algal ingestion rates, prosome length, and lipid mass. A General Linear Model (GLM) was used to compare fatty acid and alcohol data. Moulting data were assembled into binary format (“Moulted = 1”, “Not-moulted = 0”), and a Bernoulli GLM used to assess the probability of copepod moulting for each treatment, with homogeneity among replicates determined using “binomial” family and “logit” link functions. Model assumptions were validated by extracting deviance residuals and examining their distribution. Data are presented as mean ± standard error, with statistical significance assigned where P < 0.05.

Results

ARTICLE SECTIONS
Jump To

Microplastic Uptake

Following a 2 h exposure, nylon fibers and granules were visualized in the intestinal tracts and faecal pellets of the juvenile copepods, confirming uptake and egestion (Figure 1).

Figure 1

Figure 1. Ingestion and egestion of microplastics by juvenile Calanus finmarchicus: (A) nylon fibers (10 × 30 μm) in the intestinal tract; (B) nylon granules (10–30 μm) in the faecal pellets. Nylon microplastics were fluorescently dyed with Nile Red and visualized under stereo microscope (Leica MZAPO/Nikon DigitalSight Fi1-U2) equipped with a Leica “green” fluorescent filter (excitation 546/10 nm, dichroic splitter 565 nm and emission OG590). Yellow bars: 100 μm.

Additive Chemical Profiling

A range of monomers, manufacturing byproducts and additives, including lubricants, stabilizers and antimicrobials, were tentatively identified (based on >85% match) in the nylon fibers (SI Table S1) and granules (SI Table S2). Four compounds were common to both plastics: the monomer caprolactam (hexano-6-lactam); the lubricants cyclomethicone 6 (dodecamethylcyclohexasiloxane) and cyclomethicone 5 (decamethylcyclopentasiloxane); and 1H-tetrazol-5-amine. The UV stabilizer benzophenone was identified in nylon fibers.

Algal Ingestion Rates

Average microalgal dimensions (SI Table S3) were used to calculate mean carbon biomass per cell values of 0.98 ng C for D. tertiolecta, 1.66 ng C for T. rotula, and 25.2 ng C for S. trochoidea. Mean microplastic concentrations in aqueous media were 46.6 fibers and 53.4 granules mL–1; mean ingestion rates for microplastics were ∼1700 fibers copepod–1 d–1 and ∼5700 granules copepod–1 d–1. Copepods exposed to both fibers and granules showed a slight (nonsignificant) increase in algal ingestion rates for D. tertiolecta (ANOVA, P = 0.30; Figure 2A). Copepods exposed to nylon fibers showed significant reductions in algal ingestion rates for T. rotula and S. trochoidea (ANOVA, P < 0.01; Figure 2B/C), whereas copepods exposed to nylon granules showed no differences in feeding rates for T. rotula (ANOVA, P = 0.44) or S. trochoidea (ANOVA, P = 0.87). Overall, copepods exposed to fibers showed an average 40% reduction in algal ingestion (ANOVA, P = 0.07; Figure 2D). No difference in total algal ingestion rates were observed for copepods exposed to nylon granules (ANOVA, P = 0.88).

Figure 2

Figure 2. Juvenile Calanus finmarchicus ingestion rates (μg C individual–1 day–1) for: (A) D. tertiolecta; (B) T. rotula; (C) S. trochoidea; and (D) total algae. Results displayed as mean with standard error. * denotes significant different from control (P < 0.05).

Prosome Length

There was no significant difference in the prosome length of juvenile (ANOVA, P = 0.65), female (ANOVA, P = 0.09), or male (ANOVA, P = 0.58) copepods exposed to either type of microplastic (SI Figure S3).

Total Lipid Mass and Lipid Profiles

The average lipid mass of juvenile copepods at the start of the experiment was 66.7 ± 5.5 μg. Significant lipid accumulation was observed in juvenile copepods in the control and fiber treatments (ANOVA, P < 0.01), but not the granule treatment (ANOVA, P = 0.63; Figure 3). The average lipid content of juvenile copepods in the control treatment (100.4 ± 7.0 μg) exceeded that of copepods in the granule treatment (77.2 ± 6.3 μg), however this difference was not statistically significant (ANOVA, P = 0.07; Figure 3). Furthermore, no significant differences were observed in the lipid mass of female (ANOVA, P = 0.42) or male (ANOVA, P = 0.96) copepods. There was no significant difference in juvenile copepod fatty acid (GLM, control-fibers, P = 0.09; GLM, control-granules P = 0.34; SI Figure S4) or fatty alcohol (GLM, control-fibers P = 0.80; GLM, control-granules P = 0.90; SI Figure S5) composition. For individual fatty acids and alcohols, the prevalence of palmitoleic acid (16:1 (n–7)) and linoleic acid (18:2 (n–6)) were significantly reduced in the fiber treatment (GLM, P < 0.05), and the prevalence of palmityl alcohol (16:0) significantly reduced and arachidyl alcohol (20:1) significantly increased in the granule treatment (GLM, P < 0.05).

Figure 3

Figure 3. Impact of fibrous and particulate microplastics on lipid accumulation in C. finmarchicus. The lipid mass (μg) of juvenile (CV), female and male C. finmarchicus prior to the start of experiment (Tzero; checked pattern) and following a 6-day exposure period. Treatments: control (white), nylon fibers (light gray), and nylon granules (dark gray). Letters show significant difference between treatments (ANOVA with posthoc Tukey).

Moulting

Across Days 0–4 there was no evidence of moulting in any treatment (Figure 4). The Bernoulli GLM showed the “replicate” factor was not significantly different among treatments for Day 5 (b = 0.03, z = 0.51, P = 0.61) or Day 6 (b = −0.07, z = −0.84, P = 0.40) and was therefore excluded from further analyses. On Day 5, 9.0 ± 3.2% of copepods had moulted in the control treatment, while a significantly greater proportion of copepods had moulted in the nylon fiber treatment (36.1 ± 8.6%; Bernoulli GLM, b = 1.47, z = 0.5, P < 0.01) and nylon granule treatments (34.4 ± 10.7%; Bernoulli GLM, b = 1.42, z = 0.51, P < 0.01; Figure 4). The proportion of copepods reaching adulthood increased between Days 5 and 6 for all treatments. On Day 6 30.6 ± 9.5% of controls had moulted, with a higher proportion of moults in copepods exposed to nylon fibers (52.3 ± 7.5%; Bernoulli GLM, b = 0.86, z = 1.84, P = 0.07) and a statistically significant higher proportion of moults in copepods exposed to nylon granules (55.9 ± 9.9%; Bernoulli GLM, b = 1.14, z = 0.49, P < 0.05).

Figure 4

Figure 4. Impact of fibrous and particulate microplastics on moulting in C. finmarchicus. Percentage of copepods which moulted on each day of the exposure period. Treatments: control (white), nylon fibers (light gray), and nylon granules (dark gray). Letters denote significant difference (in moulting each day) between treatments (P < 0.05).

Discussion

ARTICLE SECTIONS
Jump To

Our study reveals that microplastic exposure can impact upon prey selectivity, feeding, lipid accumulation, and moulting in a keystone marine organism. Microplastic shape influenced bioavailability and observed effects, with exposure to nylon fibers causing significant shifts in prey selectivity resulting in a 40% decrease in algal ingestion rates, and nylon granules negatively affecting lipid accumulation. We further observed that both microplastic types caused premature moulting, although the mechanism underpinning this developmental shift remains unclear. These results add to the growing evidence that at high concentrations, marine microplastics can significantly affect copepod feeding and health, with potential knock-on effects for marine food webs and ecological processes in which copepods play vital roles.

Uptake

Ingestion and egestion of both nylon microplastic fibers and granules was observed in juvenile C. finmarchicus. The capacity for copepods and other zooplankton to ingest spherical polystyrene beads under laboratory conditions has been widely demonstrated, (34) and juvenile (CV), female and male C. finmarchicus have been shown to readily ingest and egest polystyrene fragments (<30 μm diameter). (30) Furthermore, irregularly shaped and fibrous microplastics have been identified in wild copepods sampled from the natural environment. (31,32)

Feeding

When exposed to the fibrous microplastics, juvenile C. finmarchicus demonstrated substantial shifts in feeding, with significantly reduced ingestion rates for the largest algae T. rotula (19 × 24 μm) and S. trochoidea (29 × 34 μm), contributing to a 40% decrease in ingested biomass compared with controls. A comparable shift in feeding selectivity was observed in the temperate copepod Calanus helgolandicus, in which exposure to 20 μm polystyrene beads resulted in a preferential shift toward smaller algae, similarly resulting in a 40% reduction in ingested biomass. (22) In mixed algal assemblages C. finmarchicus typically predate on larger, nutritionally valuable prey (e.g., diatoms, dinoflagellates, and ciliates), (46,47) for which they display higher filtration rates and feeding efficiencies. (48,49) This preference for larger algae is evident for copepods in the control and granule treatments, with >50% of ingested biomass derived from S. trochoidea. However, for copepods exposed to fibers the majority of ingested biomass came from the smallest algae, D. tertiolecta (9 × 13 μm). This shift in prey selectivity would therefore suggest copepods are avoiding microalgae of similar shape (i.e., chain-forming D. tertiolecta) and size (i.e., S. trochoidea) to the nylon fibers (10 × 30 μm). This hypothesis is further supported by our finding that fibers were ingested far less readily than granules. Why this is the case is currently unclear. Perhaps their elongated shape make fibers harder to capture, handle, and ingest, or, when consumed, fibers are more prone to causing physical damage owing to their sharp edges (Supporting Information, Figure S1); conversely, granules are relatively spherical in shape, and are likely handled similarly to naturally occurring particulates (e.g., pumice, wood, black carbon, and silt) to which copepods are well adapted. The risks microplastic fibers pose to biota is relatively underexplored, however exposure studies have identified that in the freshwater zooplankton Daphnia magna and Gammarus fossasrum ingestion of synthetic fibers resulted in early mortality (50) and impaired feeding (51) respectively.

Lipids

In juvenile C. finmarchicus (CV), approximately 40% of energy derived from their food goes toward the buildup of their lipid store. (49) On the basis of the observed reduction in feeding in juvenile C. finmarchicus exposed to microplastic fibers and the shift to smaller, less nutritious algae, it was anticipated that the lipid mass of these copepods would be negatively affected; furthermore, we surmised that a shift in feeding may result in an altered lipid profile. Yet, there was no significant difference in the total lipid mass of juvenile, female, or male copepods at the end of the exposure period, nor were the lipid profiles of the juvenile copepods significantly altered. Given that a nonlimiting supply of food was provided to the copepods, it is plausible that even with a 40% reduction in ingested biomass that the juvenile C. finmarchicus still consumed sufficient energy to continue laying down their lipid reserves. Certainly, high latitude zooplankton can display a range of strategies to survive periods of low food availability, (52) and C. finmarchicus exhibit far greater starvation tolerance (>21 days) than temperate species. (39)
We did observe that lipid accumulation was stymied in preadult copepods exposed to nylon granules. This was surprising given that nylon granules caused no impact on feeding rate. This intriguing result might be explained by the substantially higher ingestion rate for granules, as compared with fibers: high microplastic loads in the intestinal tract could limit assimilation efficiencies, as observed in the freshwater amphipod G. fossarum; (53) alternatively, higher microplastic loads could lead to greater quantities of toxic additives or monomers permeating from the microplastic into tissues. (51)
Lipid mass is directly related to the depth at which copepods can successfully descend during diapause; smaller lipid reserves would result in overwintering at shallower depths leaving these copepods more prone to predation. (54) There are also repercussions for the wider marine food web, as a reduced lipid content would make these copepods less nutritionally valuable as a food source for higher trophic organisms including commercially important fish species and megafauna. (36)

Moulting

Our study further identified that copepods exposed to nylon microplastics moulted significantly earlier than copepods in the control treatment. Juvenile C. finmarchicus have a flexible life history, where they can either enter diapause or moult into their adult life stage. Tarrant et al. (40) notes, “the factors that regulate this developmental plasticity are poorly understood”, although lipid profiles, temperature, light, food availability, and endogenous clocks have all been mooted as contributing factors in diapause. (55) Cultured C. finmarchicus do not initiate diapause, instead undergoing morphological changes, including gonad maturation, tooth formation, and apolysis (separation of the cuticle from the epidermis), prior to their terminal moult. (56) Reduced feeding and stymied lipid accumulation may both have contributed to earlier moulting; however endocrine disruption might also have played a role. A transcriptomic evaluation of juvenile C. finmarchicus (CV) has identified an array of genes linked to moulting, activated by an ecdysteroid hormone signaling cascade. (40) A range of endocrine disrupting compounds have been shown to interfere with ecdysteroid pathways and affect moulting in crustacea; (57) for example, estrogenic compounds have been shown to inhibit or delay moulting in the copepod Acartia tonsa, (58) while the pesticide emamectin benzoate has been demonstrated to cause premature moulting in American lobster, Homarus americanus. (59) Chemical analysis revealed the nylon microplastics used in these exposures contain compounds that may cause toxicity or endocrine disruption—although it should be noted this analysis does not tell us which compounds, nor how much, could be expected to leach from the nylon either in seawater or the intestinal tract of a copepod. For example, the UV-stabilizer benzophenone, identified in the nylon fibers, has been shown to increase DNA methylation and significantly reduce egg hatching success in the marine copepod Gladioferens pectinatus, (60) and act as an oestradiol agonist in rats (61) and fish. (62,63) It is crucial to recognize that plastics are not an inert material, but a complex mixture of polymers containing a wide spectrum of compounds that have the potential to leach out. (64) Given the capacity for these compounds to cause endocrine disruption or toxicity, it is crucial that chemical profiling of microplastics used in toxicity testing becomes more commonplace.

Environmental Relevance

In this exposure study we demonstrate that microplastics have the capacity to reduce feeding, stymie lipid accumulation, and trigger premature moulting in a boreal copepod. It should be noted that microplastic concentrations used in our exposure studies exceed those currently observed in the marine environment—although we would also highlight there is very little environmental data relating to concentrations of particles 10–30 μm in size owing to the technical challenges of sampling, extracting and identifying plastic particles of this size and where data are available, it suggests the smaller the microplastics the higher the concentration becomes. (65−68) While it is important the field of microplastics research shifts toward better understanding the risks environmentally relevant concentrations of microplastic pose to marine life, at this stage it remains essential to build a clearer picture of the modes of action by which microplastics can cause harm, identify relevant end points, and gauge the sensitivity of different life-stages and species. (69) Such knowledge is key in establishing probable and no-effect thresholds for risk assessment. In this study, the use of preadult copepods highlights that microplastics can affect moulting, which will inform future experimental work. As our results demonstrate, the shape and chemical profile of a microplastic can influence bioavailability and toxicity, and we would therefore promote the call for future studies to better incorporate a greater diversity of environmentally relevant microplastics.

Supporting Information

ARTICLE SECTIONS
Jump To

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.9b01853.

  • Images of the microalgae, microplastics, and copepods; chemical data for the nylon fibers and granules; data relating to the size and shape of microalgae; and fatty acid and alcohol data for copepods in control, fiber, and granule treatments (PDF)

Terms & Conditions

Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

Author Information

ARTICLE SECTIONS
Jump To

  • Corresponding Authors
  • Authors
    • Rachel Coppock - Marine Ecology and Biodiversity Group, Plymouth Marine Laboratory, Plymouth PL1 3DH, United KingdomCollege of Life and Environmental Sciences: Biosciences, University of Exeter, Exeter EX4 4QD, United Kingdom
    • Dag Altin - BioTrix, Trondheim NO-7022, Norway
    • Sarah Reed - Scottish Association of Marine Science, Scottish Marine Institute, Oban PA37 1QA, United Kingdom
    • David W. Pond - Scottish Association of Marine Science, Scottish Marine Institute, Oban PA37 1QA, United KingdomInstitute of Aquaculture, University of Stirling, Stirling FK9 4LA, United Kingdom
    • Lisbet Sørensen - SINTEF Ocean AS, Trondheim NO-7465, Norway
    • Tamara S. Galloway - College of Life and Environmental Sciences: Biosciences, University of Exeter, Exeter EX4 4QD, United Kingdom
    • Andy M. Booth - SINTEF Ocean AS, Trondheim NO-7465, NorwayOrcidhttp://orcid.org/0000-0002-4702-2210
  • Notes
    The authors declare no competing financial interest.

Acknowledgments

ARTICLE SECTIONS
Jump To

Funding was provided by the Natural Environment Research Council (NE/L007010, NE/L002582/1, NE/P006280/1, and NE/L002434/1), the JPI Oceans project “PLASTOX” (direct and indirect ecotoxicological impacts of microplastics on marine organisms; Research Council of Norway, grant no. 257479), and the RCN project “MICROFIBRE” (grant no. 268404). Our thanks to Iurgi Salaberria for assistance in planning the studies and providing access to facilities at NTNU.

References

ARTICLE SECTIONS
Jump To

This article references 69 other publications.

  1. 1
    Hartmann, N. B.; Hüffer, T.; Thompson, R.; Hassellöv, M.; Verschoor, A.; Daugaard, A.; Rist, S.; Karlsson, T. M.; Brennholt, N.; Cole, M.; Herrling, M.; Heß, M.; Ivleva, N.; Lusher, A.; Wagner, M. Are we speaking the same language? Recommendations for a definition and categorization framework for plastic debris. Environ. Sci. Technol. 2019, 53, 10391047,  DOI: 10.1021/acs.est.8b05297
  2. 2
    Lusher, A. Microplastics in the marine environment: distribution, interactions and effects. In Marine Anthropogenic Litter; Bergmann, M., Gutow, L., Klages, M., Eds.; Springer: 2015; pp 245307.
  3. 3
    Cole, M.; Lindeque, P.; Halsband, C.; Galloway, T. S. Microplastics as contaminants in the marine environment: A review. Mar. Pollut. Bull. 2011, 62, 25882597,  DOI: 10.1016/j.marpolbul.2011.09.025
  4. 4
    Weinstein, J. E.; Crocker, B. K.; Gray, A. D. From macroplastic to microplastic: Degradation of high-density polyethylene, polypropylene, and polystyrene in a salt marsh habitat. Environ. Toxicol. Chem. 2016, 35 (7), 16321640,  DOI: 10.1002/etc.3432
  5. 5
    Eriksen, M.; Lebreton, L. C.; Carson, H. S.; Thiel, M.; Moore, C. J.; Borerro, J. C.; Galgani, F.; Ryan, P. G.; Reisser, J. Plastic Pollution in the World’s Oceans: More than 5 Trillion Plastic Pieces Weighing over 250,000 Tons Afloat at Sea. PLoS One 2014, 9 (12), e111913,  DOI: 10.1371/journal.pone.0111913
  6. 6
    Andrady, A. L. Persistence of plastic litter in the oceans. In Marine Anthropogenic Litter; Bergmann, M., Gutow, L., Klages, M., Eds.; Springer: 2015; pp 5772.
  7. 7
    FAO Microplastics in Fisheries and Aquaculture: Status of Knowledge on Their Occurrence and Implications for Aquatic Organisms and Food Safety; FAO: Rome, Italy, 2017; Vol. 615.
  8. 8
    Steer, M.; Cole, M.; Thompson, R. C.; Lindeque, P. K. Microplastic ingestion in fish larvae in the western English Channel. Environ. Pollut. 2017, 226, 250259,  DOI: 10.1016/j.envpol.2017.03.062
  9. 9
    Catarino, A. I.; Macchia, V.; Sanderson, W. G.; Thompson, R. C.; Henry, T. B. Low levels of microplastics (MP) in wild mussels indicate that MP ingestion by humans is minimal compared to exposure via household fibres fallout during a meal. Environ. Pollut. 2018, 237, 675684,  DOI: 10.1016/j.envpol.2018.02.069
  10. 10
    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 (15), 88188824,  DOI: 10.1021/es400931b
  11. 11
    Lusher, A.; McHugh, M.; Thompson, R. Occurrence of microplastics in the gastrointestinal tract of pelagic and demersal fish from the English Channel. Mar. Pollut. Bull. 2013, 67 (1–2), 9499,  DOI: 10.1016/j.marpolbul.2012.11.028
  12. 12
    Duncan, E. M.; Broderick, A. C.; Fuller, W. J.; Galloway, T. S.; Godfrey, M. H.; Hamann, M.; Limpus, C. J.; Lindeque, P. K.; Mayes, A. G.; Omeyer, L. C. Microplastic ingestion ubiquitous in marine turtles. Global change biology 2019, 25 (2), 744752,  DOI: 10.1111/gcb.14519
  13. 13
    Nelms, S.; Barnett, J.; Brownlow, A.; Davison, N.; Deaville, R.; Galloway, T.; Lindeque, P.; Santillo, D.; Godley, B. Microplastics in marine mammals stranded around the British coast: ubiquitous but transitory?. Sci. Rep. 2019, 9 (1), 1075,  DOI: 10.1038/s41598-018-37428-3
  14. 14
    Meeker, J. D.; Sathyanarayana, S.; Swan, S. H. Phthalates and other additives in plastics: human exposure and associated health outcomes. Philos. Trans. R. Soc., B 2009, 364 (1526), 20972113,  DOI: 10.1098/rstb.2008.0268
  15. 15
    Johansen, M. P.; Prentice, E.; Cresswell, T.; Howell, N. Initial data on adsorption of Cs and Sr to the surfaces of microplastics with biofilm. J. Environ. Radioact. 2018, 190, 130133,  DOI: 10.1016/j.jenvrad.2018.05.001
  16. 16
    Zuo, L.-Z.; Li, H.-X.; Lin, L.; Sun, Y.-X.; Diao, Z.-H.; Liu, S.; Zhang, Z.-Y.; Xu, X.-R. Sorption and desorption of phenanthrene on biodegradable poly (butylene adipate co-terephtalate) microplastics. Chemosphere 2019, 215, 2532,  DOI: 10.1016/j.chemosphere.2018.09.173
  17. 17
    Muller-Karanassos, C.; Turner, A.; Arundel, W.; Vance, T.; Lindeque, P. K.; Cole, M. Antifouling paint particles in intertidal estuarine sediments from southwest England and their ingestion by the harbour ragworm, Hediste diversicolor. Environ. Pollut. 2019, 249, 163170,  DOI: 10.1016/j.envpol.2019.03.009
  18. 18
    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 (23–24), 13691371,  DOI: 10.1080/15287394.2017.1385046
  19. 19
    Wright, S.; Rowe, D.; Thompson, R. C.; Galloway, T. S. Microplastic ingestion decreases energy reserves in marine worms. Curr. Biol. 2013, 23 (23), 10311033,  DOI: 10.1016/j.cub.2013.10.068
  20. 20
    Wegner, A.; Besseling, E.; Foekema, E.; Kamermans, P.; Koelmans, A. Effects of nanopolystyrene on the feeding behavior of the blue mussel (Mytilus edulis L.). Environ. Toxicol. Chem. 2012, 31 (11), 24902497,  DOI: 10.1002/etc.1984
  21. 21
    Besseling, E.; Wegner, A.; Foekema, E. M.; van den Heuvel-Greve, M. J.; Koelmans, A. A. Effects of Microplastic on Fitness and PCB Bioaccumulation by the Lugworm Arenicola marina (L.). Environ. Sci. Technol. 2013, 47 (1), 593600,  DOI: 10.1021/es302763x
  22. 22
    Cole, M.; Lindeque, P.; Fileman, E.; Halsband, C.; Galloway, T. The impact of polystyrene microplastics on feeding, function and fecundity in the marine copepod Calanus helgolandicus. Environ. Sci. Technol. 2015, 49 (2), 11301137,  DOI: 10.1021/es504525u
  23. 23
    Sussarellu, R.; Suquet, M.; Thomas, Y.; Lambert, C.; Fabioux, C.; Pernet, M. E. J.; Le Goïc, N.; Quillien, V.; Mingant, C.; Epelboin, Y. Oyster reproduction is affected by exposure to polystyrene microplastics. Proc. Natl. Acad. Sci. U. S. A. 2016, 113 (9), 24302435,  DOI: 10.1073/pnas.1519019113
  24. 24
    Cole, M.; Lindeque, P. K.; Fileman, E.; Clark, J.; Lewis, C.; Halsband, C.; Galloway, T. S. Microplastics alter the properties and sinking rates of zooplankton faecal pellets. Environ. Sci. Technol. 2016, 50, 32393246,  DOI: 10.1021/acs.est.5b05905
  25. 25
    Galloway, T. S.; Cole, M.; Lewis, C. Interactions of microplastic debris throughout the marine ecosystem. Nature Ecology & Evolution 2017, 1 (5), s41559,  DOI: 10.1038/s41559-017-0116
  26. 26
    Irigoien, X.; Harris, R. P.; Verheye, H. M.; Joly, P.; Runge, J.; Starr, M.; Pond, D.; Campbell, R.; Shreeve, R.; Ward, P. Copepod hatching success in marine ecosystems with high diatom concentrations. Nature 2002, 419 (6905), 387389,  DOI: 10.1038/nature01055
  27. 27
    Cole, M.; Lindeque, P.; Fileman, E.; Halsband, C.; Goodhead, R.; Moger, J.; Galloway, T. S. Microplastic ingestion by zooplankton. Environ. Sci. Technol. 2013, 47 (12), 66466655,  DOI: 10.1021/es400663f
  28. 28
    Setälä, O.; Fleming-Lehtinen, V.; Lehtiniemi, M. Ingestion and transfer of microplastics in the planktonic food web. Environ. Pollut. 2014, 185, 7783,  DOI: 10.1016/j.envpol.2013.10.013
  29. 29
    Lee, K.-W.; Shim, W. J.; Kwon, O. Y.; Kang, J.-H. Size-Dependent Effects of Micro Polystyrene Particles in the Marine Copepod Tigriopus japonicus. Environ. Sci. Technol. 2013, 47 (19), 1127811283,  DOI: 10.1021/es401932b
  30. 30
    Vroom, R. J.; Koelmans, A. A.; Besseling, E.; Halsband, C. Aging of microplastics promotes their ingestion by marine zooplankton. Environ. Pollut. 2017, 231, 987996,  DOI: 10.1016/j.envpol.2017.08.088
  31. 31
    Sun, X.; Li, Q.; Zhu, M.; Liang, J.; Zheng, S.; Zhao, Y. Ingestion of microplastics by natural zooplankton groups in the northern South China Sea. Mar. Pollut. Bull. 2017, 115 (1–2), 217224,  DOI: 10.1016/j.marpolbul.2016.12.004
  32. 32
    Desforges, J.-P. W.; Galbraith, M.; Ross, P. S. Ingestion of Microplastics by Zooplankton in the Northeast Pacific Ocean. Arch. Environ. Contam. Toxicol. 2015, 69 (4), 320330,  DOI: 10.1007/s00244-015-0172-5
  33. 33
    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 (11), 30743080,  DOI: 10.1002/etc.3881
  34. 34
    Botterell, Z. L.; Beaumont, N.; Dorrington, T.; Steinke, M.; Thompson, R. C.; Lindeque, P. K. Bioavailability and effects of microplastics on marine zooplankton: A review. Environ. Pollut. 2019, 245, 98110,  DOI: 10.1016/j.envpol.2018.10.065
  35. 35
    Paul-Pont, I.; Tallec, K.; Gonzalez-Fernandez, C.; Lambert, C.; Vincent, D.; Mazurais, D.; Zambonino-Infante, J.-L.; Brotons, G.; Lagarde, F.; Fabioux, C. Constraints and priorities for conducting experimental exposures of marine organisms to microplastics. Front. Mar. Sci. 2018, 5 (252) DOI: 10.3389/fmars.2018.00252 .
  36. 36
    Melle, W.; Runge, J.; Head, E.; Plourde, S.; Castellani, C.; Licandro, P.; Pierson, J.; Jonasdottir, S.; Johnson, C.; Broms, C. The North Atlantic Ocean as habitat for Calanus finmarchicus: Environmental factors and life history traits. Prog. Oceanogr. 2014, 129, 244284,  DOI: 10.1016/j.pocean.2014.04.026
  37. 37
    Pond, D. W. The physical properties of lipids and their role in controlling the distribution of zooplankton in the oceans. J. Plankton Res. 2012, 34 (6), 443453,  DOI: 10.1093/plankt/fbs027
  38. 38
    Marker, T.; Andreassen, P.; Arashkewich, E.; Hansen, B. W. Lipid deposition and sexual maturation in cohorts of Calanus finmarchicus (Gunnerus) originating from Bergen (60 N) and Tromsø (69 N) reared in Tromsø, Norway. Mar. Biol. 2003, 143 (2), 283296,  DOI: 10.1007/s00227-003-1089-5
  39. 39
    Lee, R. F.; Hagen, W.; Kattner, G. Lipid storage in marine zooplankton. Mar. Ecol.: Prog. Ser. 2006, 307, 273306,  DOI: 10.3354/meps307273
  40. 40
    Tarrant, A. M.; Baumgartner, M. F.; Hansen, B. H.; Altin, D.; Nordtug, T.; Olsen, A. J. Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus. Front. Zool. 2014, 11 (1), 91,  DOI: 10.1186/s12983-014-0091-8
  41. 41
    Jones, R. H.; Flynn, K. J.; Anderson, T. R. Effect of food quality on carbon and nitrogen growth efficiency in the copepod Acartia tonsa. Mar. Ecol.: Prog. Ser. 2002, 235, 147156,  DOI: 10.3354/meps235147
  42. 42
    Cole, M., Novel method for preparing microplastic fibres. Sci. Rep. 2016 DOI: 10.1038/srep34519 .
  43. 43
    Frost, B. W. Effect of size and concentration of food particles on the feeding behaviour of the marine planktoinic copepod Calanus pacificus. Limnol. Oceanogr. 1972, 17, 805815,  DOI: 10.4319/lo.1972.17.6.0805
  44. 44
    Folch, J.; Lees, M.; Sloane Stanley, G. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 1957, 226 (1), 497509
  45. 45
    R. C. Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2016.
  46. 46
    Meyer-Harms, B.; Irigoien, X.; Head, R.; Harris, R. Selective feeding on natural phytoplankton by Calanus finmarchicus before, during, and after the 1997 spring bloom in the Norwegian Sea. Limnol. Oceanogr. 1999, 44 (1), 154165,  DOI: 10.4319/lo.1999.44.1.0154
  47. 47
    Leiknes, Ø.; Striberny, A.; Tokle, N. E.; Olsen, Y.; Vadstein, O.; Sommer, U. Feeding selectivity of Calanus finmarchicus in the Trondheimsfjord. J. Sea Res. 2014, 85, 292299,  DOI: 10.1016/j.seares.2013.05.012
  48. 48
    Meyer, B.; Irigoien, X.; Graeve, M.; Head, R.; Harris, R. Feeding rates and selectivity among nauplii, copepodites and adult females of Calanus finmarchicus and Calanus helgolandicus. Helgoland Marine Research 2002, 56 (3), 169176,  DOI: 10.1007/s10152-002-0105-3
  49. 49
    Marshall, S.; Orr, A. On the biology of Calanus finmarchicus VIII. Food uptake, assimilation and excretion in adult and stage V Calanus. J. Mar. Biol. Assoc. U. K. 1955, 34 (3), 495529,  DOI: 10.1017/S0025315400008778
  50. 50
    Jemec, A.; Horvat, P.; Kunej, U.; Bele, M.; Kržan, A. Uptake and effects of microplastic textile fibers on freshwater crustacean Daphnia magna. Environ. Pollut. 2016, 219, 201209,  DOI: 10.1016/j.envpol.2016.10.037
  51. 51
    Bakir, A.; Rowland, S. J.; Thompson, R. C. Enhanced desorption of persistent organic pollutants from microplastics under simulated physiological conditions. Environ. Pollut. 2014, 185, 1623,  DOI: 10.1016/j.envpol.2013.10.007
  52. 52
    Litchman, E.; Ohman, M. D.; Kiørboe, T. Trait-based approaches to zooplankton communities. J. Plankton Res. 2013, 35 (3), 473484,  DOI: 10.1093/plankt/fbt019
  53. 53
    Blarer, P.; Burkhardt-Holm, P. Microplastics affect assimilation efficiency in the freshwater amphipod Gammarus fossarum. Environ. Sci. Pollut. Res. 2016, 23 (23), 2352223532,  DOI: 10.1007/s11356-016-7584-2
  54. 54
    Jónasdóttir, S. H. Lipid content of Calanus finmarchicus during overwintering in the Faroe–Shetland Channel. Fisheries Oceanography 1999, 8, 6172,  DOI: 10.1046/j.1365-2419.1999.00003.x
  55. 55
    Häfker, N. S.; Teschke, M.; Last, K. S.; Pond, D. W.; Hüppe, L.; Meyer, B. Calanus finmarchicus seasonal cycle and diapause in relation to gene expression, physiology, and endogenous clocks. Limnol. Oceanogr. 2018, 63 (6), 28152838,  DOI: 10.1002/lno.11011
  56. 56
    Crain, J. A.; Miller, C. B. Effects of starvation on intermolt development in Calanus finmarchicus copepodites: a comparison between theoretical models and field studies. Deep Sea Res., Part II 2001, 48 (1–3), 551566,  DOI: 10.1016/S0967-0645(00)00078-3
  57. 57
    Rodríguez, E. M.; Medesani, D. A.; Fingerman, M. Endocrine disruption in crustaceans due to pollutants: a review. Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol. 2007, 146 (4), 661671,  DOI: 10.1016/j.cbpa.2006.04.030
  58. 58
    Andersen, H. R.; Wollenberger, L.; Halling-Sørensen, B.; Kusk, K. O. Development of copepod nauplii to copepodites—a parameter for chronic toxicity including endocrine disruption. Environ. Toxicol. Chem. 2001, 20 (12), 28212829,  DOI: 10.1002/etc.5620201222
  59. 59
    Waddy, S.; Burridge, L.; Hamilton, M.; Mercer, S.; Aiken, D.; Haya, K. Rapid communication/communication rapide emamectin benzoate induces molting in American lobster, Homarus americanus. Can. J. Fish. Aquat. Sci. 2002, 59 (7), 10961099,  DOI: 10.1139/f02-106
  60. 60
    Guyon, A.; Smith, K. F.; Charry, M. P.; Champeau, O.; Tremblay, L. A. Effects of chronic exposure to benzophenone and diclofenac on DNA methylation levels and reproductive success in a marine copepod. J. Xenobiot. 2018, 8 (1), 7674,  DOI: 10.4081/xeno.2018.7674
  61. 61
    Jarry, H.; Christoffel, J.; Rimoldi, G.; Koch, L.; Wuttke, W. Multi-organic endocrine disrupting activity of the UV screen benzophenone 2 (BP2) in ovariectomized adult rats after 5 days treatment. Toxicology 2004, 205 (1–2), 8793,  DOI: 10.1016/j.tox.2004.06.040
  62. 62
    Kim, S.; Jung, D.; Kho, Y.; Choi, K. Effects of benzophenone-3 exposure on endocrine disruption and reproduction of Japanese medaka (Oryzias latipes)—A two generation exposure study. Aquat. Toxicol. 2014, 155, 244252,  DOI: 10.1016/j.aquatox.2014.07.004
  63. 63
    Kinnberg, K. L.; Petersen, G. I.; Albrektsen, M.; Minghlani, M.; Awad, S. M.; Holbech, B. F.; Green, J. W.; Bjerregaard, P.; Holbech, H. Endocrine-disrupting effect of the ultraviolet filter benzophenone-3 in zebrafish, Danio rerio. Environ. Toxicol. Chem. 2015, 34 (12), 28332840,  DOI: 10.1002/etc.3129
  64. 64
    Rochman, C. M.; Brookson, C.; Bikker, J.; Djuric, N.; Earn, A.; Bucci, K.; Athey, S.; Huntington, A.; McIlwraith, H.; Munno, K. Rethinking microplastics as a diverse contaminant suite. Environ. Toxicol. Chem. 2019, 38 (4), 703711,  DOI: 10.1002/etc.4371
  65. 65
    de Sá, L. C.; Oliveira, M.; Ribeiro, F.; Rocha, T. L.; Futter, M. N. Studies of the effects of microplastics on aquatic organisms: What do we know and where should we focus our efforts in the future?. Sci. Total Environ. 2018, 645, 10291039,  DOI: 10.1016/j.scitotenv.2018.07.207
  66. 66
    Lusher, A.; Welden, N.; Sobral, P.; Cole, M. Sampling, isolating and identifying microplastics ingested by fish and invertebrates. Anal. Methods 2017, 9, 13461360,  DOI: 10.1039/C6AY02415G
  67. 67
    Erni-Cassola, G.; Zadjelovic, V.; Gibson, M. I.; Christie-Oleza, J. A. Distribution of plastic polymer types in the marine environment; A meta-analysis. J. Hazard. Mater. 2019, 369, 691698,  DOI: 10.1016/j.jhazmat.2019.02.067
  68. 68
    Enders, K.; Lenz, R.; Stedmon, C. A.; Nielsen, T. G. Abundance, size and polymer composition of marine microplastics≥ 10 μm in the Atlantic Ocean and their modelled vertical distribution. Mar. Pollut. Bull. 2015, 100 (1), 7081,  DOI: 10.1016/j.marpolbul.2015.09.027
  69. 69
    Huvet, A.; Paul-Pont, I.; Fabioux, C.; Lambert, C.; Suquet, M.; Thomas, Y.; Robbens, J.; Soudant, P.; Sussarellu, R. Reply to Lenz et al.: Quantifying the smallest microplastics is the challenge for a comprehensive view of their environmental impacts. Proc. Natl. Acad. Sci. U. S. A. 2016, 113 (29), E4123E4124,  DOI: 10.1073/pnas.1607221113

Cited By

This article is cited by 139 publications.

  1. Taghi Moazzenzade, Jurriaan Huskens, Serge G. Lemay. Utilizing the Oxygen Reduction Reaction in Particle Impact Electrochemistry: A Step toward Mediator-Free Digital Electrochemical Sensors. ACS Omega 2023, 8 (34) , 31265-31270. https://doi.org/10.1021/acsomega.3c03576
  2. Jiaji Sun, Shiyi Yang, Guang-Jie Zhou, Kai Zhang, Yichun Lu, Qianqian Jin, Paul K. S. Lam, Kenneth M. Y. Leung, Yuhe He. Release of Microplastics from Discarded Surgical Masks and Their Adverse Impacts on the Marine Copepod Tigriopus japonicus. Environmental Science & Technology Letters 2021, 8 (12) , 1065-1070. https://doi.org/10.1021/acs.estlett.1c00748
  3. Antonio Sarno, Kjell Olafsen, Stephan Kubowicz, Fuad Karimov, Shannen T. L. Sait, Lisbet Sørensen, Andy M. Booth. Accelerated Hydrolysis Method for Producing Partially Degraded Polyester Microplastic Fiber Reference Materials. Environmental Science & Technology Letters 2021, 8 (3) , 250-255. https://doi.org/10.1021/acs.estlett.0c01002
  4. Wei Zou, Mengli Xia, Kai Jiang, Zhiguo Cao, Xingli Zhang, Xiangang Hu. Photo-Oxidative Degradation Mitigated the Developmental Toxicity of Polyamide Microplastics to Zebrafish Larvae by Modulating Macrophage-Triggered Proinflammatory Responses and Apoptosis. Environmental Science & Technology 2020, 54 (21) , 13888-13898. https://doi.org/10.1021/acs.est.0c05399
  5. Zara L. R. Botterell, Nicola Beaumont, Matthew Cole, Frances E. Hopkins, Michael Steinke, Richard C. Thompson, Penelope K. Lindeque. Bioavailability of Microplastics to Marine Zooplankton: Effect of Shape and Infochemicals. Environmental Science & Technology 2020, 54 (19) , 12024-12033. https://doi.org/10.1021/acs.est.0c02715
  6. Vera N. de Ruijter, Paula E. Redondo-Hasselerharm, Todd Gouin, Albert A. Koelmans. Quality Criteria for Microplastic Effect Studies in the Context of Risk Assessment: A Critical Review. Environmental Science & Technology 2020, 54 (19) , 11692-11705. https://doi.org/10.1021/acs.est.0c03057
  7. Jue Li, Xiaowei Zheng, Xianglin Liu, Liangliang Zhang, Shun Zhang, Yanyao Li, Weizhen Zhang, Qihui Li, Yuqiang Zhao, Xunfeng Chen, Xiangrong Wang, Honghui Huang, Zhengqiu Fan. Effect and mechanism of microplastics exposure against microalgae: Photosynthesis and oxidative stress. Science of The Total Environment 2023, 905 , 167017. https://doi.org/10.1016/j.scitotenv.2023.167017
  8. Krishan Kumar, Reddicherla Umapathi, Seyed Majid Ghoreishian, Jitendra N. Tiwari, Seung Kyu Hwang, Yun Suk Huh, Pannuru Venkatesu, Nagaraj P. Shetti, Tejraj M. Aminabhavi. Microplastics and biobased polymers to combat plastics waste. Chemosphere 2023, 341 , 140000. https://doi.org/10.1016/j.chemosphere.2023.140000
  9. Kefu Wang, Kangkang Wang, Yaoyao Chen, Siqi Liang, Yi Zhang, Changyan Guo, Wei Wang, Jide Wang. Desorption of sulfamethoxazole from polyamide 6 microplastics: Environmental factors, simulated gastrointestinal fluids, and desorption mechanisms. Ecotoxicology and Environmental Safety 2023, 264 , 115400. https://doi.org/10.1016/j.ecoenv.2023.115400
  10. Yiting Pan, Jin Qian, Xiaowan Ma, Wei Huang, James Kar-Hei Fang, Iqra Arif, Youji Wang, Yueyong Shang, Menghong Hu. Response of moulting genes and gut microbiome to nano-plastics and copper in juvenile horseshoe crab Tachypleus tridentatus. Marine Environmental Research 2023, 191 , 106128. https://doi.org/10.1016/j.marenvres.2023.106128
  11. Carla-Cristina Edwards, Gabriella McConnel, Daniela Ramos, Yaizeth Gurrola-Mares, Kailash Dhondiram Arole, Micah J Green, Jaclyn E Cañas-Carrell, Corey L Brelsfoard, . Microplastic ingestion perturbs the microbiome of Aedes albopictus (Diptera: Culicidae) and Aedes aegypti. Journal of Medical Entomology 2023, 60 (5) , 884-898. https://doi.org/10.1093/jme/tjad097
  12. Kamini Devi, Arun Dev Singh, Shalini Dhiman, Jaspreet Kour, Tamanna Bhardwaj, Neerja Sharma, Isha Madaan, Kanika Khanna, Puja Ohri, Amrit Pal Singh, Geetika Sirhindi, Renu Bhardwaj, Vinod Kumar. Current studies on the degradation of microplastics in the terrestrial and aquatic ecosystem. Environmental Science and Pollution Research 2023, 84 https://doi.org/10.1007/s11356-023-29640-0
  13. Vongdala Noudeng, Nguyen Van Quan, Tran Dang Xuan, Chansomphou Vathanamixay, Phengsisomboun Souvanna. Risk Assessment of Microplastics Dispersion and Accumulation in Urban Canals to the Water Environment in Vientiane Capital, Laos. Water, Air, & Soil Pollution 2023, 234 (9) https://doi.org/10.1007/s11270-023-06587-z
  14. H. Emberson-Marl, R. L. Coppock, M. Cole, B. J. Godley, N. Mimpriss, S. E. Nelms, P. K. Lindeque. Microplastics in the Arctic: a transect through the Barents Sea. Frontiers in Marine Science 2023, 10 https://doi.org/10.3389/fmars.2023.1241829
  15. Emily Rowlands, Tamara Galloway, Matthew Cole, Ceri Lewis, Christian Hacker, Victoria L. Peck, Sally Thorpe, Sabena Blackbird, George A. Wolff, Clara Manno. Scoping intergenerational effects of nanoplastic on the lipid reserves of Antarctic krill embryos. Aquatic Toxicology 2023, 261 , 106591. https://doi.org/10.1016/j.aquatox.2023.106591
  16. Jiao Li, Jie Li, Li Zhai, Kun Lu. Co-exposure of polycarbonate microplastics aggravated the toxic effects of imidacloprid on the liver and gut microbiota in mice. Environmental Toxicology and Pharmacology 2023, 101 , 104194. https://doi.org/10.1016/j.etap.2023.104194
  17. Emily Rowlands, Tamara Galloway, Matthew Cole, Victoria L. Peck, Anna Posacka, Sally Thorpe, Clara Manno. Vertical flux of microplastic, a case study in the Southern Ocean, South Georgia. Marine Pollution Bulletin 2023, 193 , 115117. https://doi.org/10.1016/j.marpolbul.2023.115117
  18. Chung Ngo Tang, Victor S. Kuwahara, Sandric Chee Yew Leong, Pak Yan Moh, Teruaki Yoshida. Effect of monsoon on microplastic bioavailability and ingestion by zooplankton in tropical coastal waters of Sabah. Marine Pollution Bulletin 2023, 193 , 115182. https://doi.org/10.1016/j.marpolbul.2023.115182
  19. Batdulam Battulga, Mariko Atarashi-Andoh, Makoto Matsueda, Jun Koarashi. Tracking the behavior and characteristics of microplastics using a multi-analytical approach: a case study in two contrasting coastal areas of Japan. Environmental Science and Pollution Research 2023, 30 (31) , 77226-77237. https://doi.org/10.1007/s11356-023-28005-x
  20. Wajid Ali, Hazrat Ali, Sayed Gillani, Philippe Zinck, Sami Souissi. Polylactic acid synthesis, biodegradability, conversion to microplastics and toxicity: a review. Environmental Chemistry Letters 2023, 21 (3) , 1761-1786. https://doi.org/10.1007/s10311-023-01564-8
  21. Huy Hoang Phan Quang, Duc Anh Dinh, Vishal Dutta, Ankush Chauhan, Sudip Kumar Lahiri, C. Gopalakrishnan, Arunkumar Radhakrishnan, Khalid Mujasam Batoo, Lan-Anh Phan Thi. Current approaches, and challenges on identification, remediation and potential risks of emerging plastic contaminants: A review. Environmental Toxicology and Pharmacology 2023, 19 , 104193. https://doi.org/10.1016/j.etap.2023.104193
  22. A.S. Shafiuddin Ahmed, Md Masum Billah, Mir Mohammad Ali, Md Khurshid Alam Bhuiyan, Laodong Guo, Mohammad Mohinuzzaman, M. Belal Hossain, M. Safiur Rahman, Md Saiful Islam, Meng Yan, Wenlong Cai. Microplastics in aquatic environments: A comprehensive review of toxicity, removal, and remediation strategies. Science of The Total Environment 2023, 876 , 162414. https://doi.org/10.1016/j.scitotenv.2023.162414
  23. Vinod Vakati, Juan Manuel Fuentes-Reinés, Pengbin Wang, Jun Wang, Steven Dodsworth. A summary of Copepoda: synthesis, trends, and ecological impacts. Journal of Oceanology and Limnology 2023, 41 (3) , 1050-1072. https://doi.org/10.1007/s00343-022-1309-9
  24. Xuan Li, Lin Lu, Shaoguo Ru, Junho Eom, Dong Wang, Samreen, Jun Wang. Nanoplastics induce more severe multigenerational life-history trait changes and metabolic responses in marine rotifer Brachionus plicatilis: Comparison with microplastics. Journal of Hazardous Materials 2023, 449 , 131070. https://doi.org/10.1016/j.jhazmat.2023.131070
  25. Saskia Kühn, Franziska King, Katja Heubel. Decreased feeding rates of the copepod Acartia tonsa when exposed to playback harbor traffic noise. Frontiers in Marine Science 2023, 10 https://doi.org/10.3389/fmars.2023.1134792
  26. Mary Claire Fibbe, Delphine Carroll, Shannon Gowans, Amy N. S. Siuda. Ingestion of microplastics by copepods in Tampa Bay Estuary, FL. Frontiers in Ecology and Evolution 2023, 11 https://doi.org/10.3389/fevo.2023.1143377
  27. Elise M. Tuuri, Sophie Catherine Leterme. How plastic debris and associated chemicals impact the marine food web: A review. Environmental Pollution 2023, 321 , 121156. https://doi.org/10.1016/j.envpol.2023.121156
  28. Siyi Zhang, Haodi Wu, Jing Hou. 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
  29. Bjørn Einar Grøsvik, Maria E. Granberg, Tanja Kögel, Amy L. Lusher, Alessio Gomiero, Halldor P. Halldorsson, Alexander Klevedal Madsen, Julia E. Baak, Hermann Dreki Guls, Kerstin Magnusson. Microplastics in Arctic invertebrates: status on occurrence and recommendations for future monitoring. Arctic Science 2023, 9 (1) , 165-175. https://doi.org/10.1139/as-2022-0004
  30. Ali Parsaeimehr, Cassandra M. Miller, Gulnihal Ozbay. Microplastics and their interactions with microbiota. Heliyon 2023, 264 , e15104. https://doi.org/10.1016/j.heliyon.2023.e15104
  31. Sumon Sarkar, Hanin Diab, Jonathan Thompson. Microplastic Pollution: Chemical Characterization and Impact on Wildlife. International Journal of Environmental Research and Public Health 2023, 20 (3) , 1745. https://doi.org/10.3390/ijerph20031745
  32. Muhammad Junaid, Shulin Liu, Guanglong Chen, Hongping Liao, Jun Wang. Transgenerational impacts of micro(nano)plastics in the aquatic and terrestrial environment. Journal of Hazardous Materials 2023, 443 , 130274. https://doi.org/10.1016/j.jhazmat.2022.130274
  33. Khaled Ziani, Corina-Bianca Ioniță-Mîndrican, Magdalena Mititelu, Sorinel Marius Neacșu, Carolina Negrei, Elena Moroșan, Doina Drăgănescu, Olivia-Teodora Preda. Microplastics: A Real Global Threat for Environment and Food Safety: A State of the Art Review. Nutrients 2023, 15 (3) , 617. https://doi.org/10.3390/nu15030617
  34. Chenxi Zhang, Chenggang Lin, Lingling Li, Mohamed Mohsen, Ting Wang, Xu Wang, Libin Zhang, Wei Huang. Single and combined effects of microplastics and cadmium on the sea cucumber Apostichopus japonicus. Marine Environmental Research 2023, 12 , 105927. https://doi.org/10.1016/j.marenvres.2023.105927
  35. Lei Wang, Yuanhui Zhu, Jie Gu, Xiaogang Yin, Liguo Guo, Lingling Qian, Lili Shi, Min Guo, Guixiang Ji. The toxic effect of bisphenol AF and nanoplastic coexposure in parental and offspring generation zebrafish. Ecotoxicology and Environmental Safety 2023, 251 , 114565. https://doi.org/10.1016/j.ecoenv.2023.114565
  36. S. Siddiqui, S. J. Hutton, J. M. Dickens, E. I. Pedersen, S. L. Harper, S. M. Brander. Natural and synthetic microfibers alter growth and behavior in early life stages of estuarine organisms. Frontiers in Marine Science 2023, 9 https://doi.org/10.3389/fmars.2022.991650
  37. Shuai Tang, Peipei Sun, Shengjia Ma, Wei Jin, Yaping Zhao. The interfacial behaviors of different arsenic species on polyethylene mulching film microplastics: Roles of the plastic additives. Journal of Hazardous Materials 2023, 442 , 130037. https://doi.org/10.1016/j.jhazmat.2022.130037
  38. Wen-Xiong Wang. Environmental toxicology of marine microplastic pollution. Cambridge Prisms: Plastics 2023, 1 https://doi.org/10.1017/plc.2023.9
  39. Adamu Yunusa Ugya, Kamel Meguellati, Abdulkadir Dauda Aliyu, Abidina Abba, Makiyyu Abdullahi Musa. Microplastic stress induce bioresource production and response in microalgae: a concise review. Environmental Pollutants and Bioavailability 2022, 34 (1) , 51-60. https://doi.org/10.1080/26395940.2022.2033138
  40. Leah M. Thornton Hampton, Susanne M. Brander, Scott Coffin, Matthew Cole, Ludovic Hermabessiere, Albert A. Koelmans, Chelsea M. Rochman. Characterizing microplastic hazards: which concentration metrics and particle characteristics are most informative for understanding toxicity in aquatic organisms?. Microplastics and Nanoplastics 2022, 2 (1) https://doi.org/10.1186/s43591-022-00040-4
  41. Samantha N. Athey, Bethanie Carney Almroth, Elise F. Granek, Paul Hurst, Alexandra G. Tissot, Judith S. Weis. Unraveling Physical and Chemical Effects of Textile Microfibers. Water 2022, 14 (23) , 3797. https://doi.org/10.3390/w14233797
  42. Prasun Goswami, Selvakumar Narasimman, Pankaj Verma, Mahua Saha, V. Suneel, Nambali Valsalan Vinithkumar, Gopal Dharani, Chayanika Rathore, Jibananand Nayak. Microplastic intrusion into the zooplankton, the base of the marine food chain: Evidence from the Arabian Sea, Indian Ocean. Science of The Total Environment 2022, , 160876. https://doi.org/10.1016/j.scitotenv.2022.160876
  43. Neha Tiwari, Deenan Santhiya, Jai Gopal Sharma. Biodegradation of micro sized nylon 6, 6 using Brevibacillus brevis a soil isolate for cleaner ecosystem. Journal of Cleaner Production 2022, 378 , 134457. https://doi.org/10.1016/j.jclepro.2022.134457
  44. Margaret Morrison, Rafael Trevisan, Prabha Ranasinghe, Greg B. Merrill, Jasmine Santos, Alexander Hong, William C. Edward, Nishad Jayasundara, Jason A. Somarelli. A growing crisis for One Health: Impacts of plastic pollution across layers of biological function. Frontiers in Marine Science 2022, 9 https://doi.org/10.3389/fmars.2022.980705
  45. Benuarda Toto, Alice Refosco, Maria O’Keeffe, Øyvind Halås Barkhald, Aurora Brønstad, Gülen Arslan Lied, Fekadu Yadetie, Anders Goksøyr, Tanja Kögel, Jutta Dierkes. Intestinal permeability and gene expression after polyethylene and polyamide microplastic ingestion in Wistar rats. Toxicology Letters 2022, 370 , 35-41. https://doi.org/10.1016/j.toxlet.2022.09.002
  46. Huipeng Nie, Huanliang Liu, Yue Shi, Wenqing Lai, Xuan Liu, Zhuge Xi, Bencheng Lin. Effects of Different Concentrations of Oil Mist Particulate Matter on Pulmonary Fibrosis In Vivo and In Vitro. Toxics 2022, 10 (11) , 647. https://doi.org/10.3390/toxics10110647
  47. Isabella Parlapiano, Francesca Biandolino, Asia Grattagliano, Andrea Ruscito, Giusy Lofrano, Giovanni Libralato, Marco Trifuoggi, Luisa Albarano, Ermelinda Prato. Multi-endpoint effects of derelict tubular mussel plastic nets on Tigriopus fulvus. Environmental Science and Pollution Research 2022, 29 (55) , 83554-83566. https://doi.org/10.1007/s11356-022-21569-0
  48. Tao Wang, Shiye Zhao, Lixin Zhu, James C. McWilliams, Luisa Galgani, Roswati Md Amin, Ryota Nakajima, Wensheng Jiang, Mengli Chen. Accumulation, transformation and transport of microplastics in estuarine fronts. Nature Reviews Earth & Environment 2022, 3 (11) , 795-805. https://doi.org/10.1038/s43017-022-00349-x
  49. Jianli Yin, Ye Ju, Honghao Qian, Jia Wang, Xiaohan Miao, Ying Zhu, Liting Zhou, Lin Ye. Nanoplastics and Microplastics May Be Damaging Our Livers. Toxics 2022, 10 (10) , 586. https://doi.org/10.3390/toxics10100586
  50. Camille Richon, Thomas Gorgues, Ika Paul-Pont, Christophe Maes. Zooplankton exposure to microplastics at global scale: Influence of vertical distribution and seasonality. Frontiers in Marine Science 2022, 9 https://doi.org/10.3389/fmars.2022.947309
  51. Surendra Pratap Singh, Pooja Sharma, Ambreen Bano, Ashok Kumar Nadda, Sunita Varjani. Microbial communities in plastisphere and free-living microbes for microplastic degradation: A comprehensive review. Green Analytical Chemistry 2022, 744 , 100030. https://doi.org/10.1016/j.greeac.2022.100030
  52. Ximena González Pisani, Julieta Sturla Lompré, Adilia Pires, Laura López Greco. Plastics in scene: A review of the effect of plastics in aquatic crustaceans. Environmental Research 2022, 212 , 113484. https://doi.org/10.1016/j.envres.2022.113484
  53. Meiting He, Muting Yan, Xiaofeng Chen, Xukun Wang, Han Gong, Wenjing Wang, Jun Wang. Bioavailability and toxicity of microplastics to zooplankton. Gondwana Research 2022, 108 , 120-126. https://doi.org/10.1016/j.gr.2021.07.021
  54. Marion Köster, Gustav-Adolf Paffenhöfer. Feeding of Marine Zooplankton on Microplastic Fibers. Archives of Environmental Contamination and Toxicology 2022, 83 (2) , 129-141. https://doi.org/10.1007/s00244-022-00948-1
  55. Zhenling Li, Min Chao, Xiaokang He, Xiaoping Lan, Chenhao Tian, Chenghong Feng, Zhenyao Shen. Microplastic bioaccumulation in estuary-caught fishery resource. Environmental Pollution 2022, 306 , 119392. https://doi.org/10.1016/j.envpol.2022.119392
  56. L. Rowenczyk, H. Cai, B. Nguyen, M. Sirois, M.-C. Côté-Laurin, N. Toupoint, A. Ismail, N. Tufenkji. From freshwaters to bivalves: Microplastic distribution along the Saint-Lawrence river-to-sea continuum. Journal of Hazardous Materials 2022, 435 , 128977. https://doi.org/10.1016/j.jhazmat.2022.128977
  57. Dilvin Yıldız, Gülce Yalçın, Boris Jovanović, David S. Boukal, Lucie Vebrová, Derya Riha, Jelena Stanković, Dimitrija Savić-Zdraković, Melisa Metin, Yasmin Naz Akyürek, Deniz Balkanlı, Nur Filiz, Djuradj Milošević, Heidrun Feuchtmayr, Jessica A. Richardson, Meryem Beklioğlu. Effects of a microplastic mixture differ across trophic levels and taxa in a freshwater food web: In situ mesocosm experiment. Science of The Total Environment 2022, 836 , 155407. https://doi.org/10.1016/j.scitotenv.2022.155407
  58. Aswathy Joshy, S.R. Krupesha Sharma, K.G. Mini. Microplastic contamination in commercially important bivalves from the southwest coast of India. Environmental Pollution 2022, 305 , 119250. https://doi.org/10.1016/j.envpol.2022.119250
  59. Anh T.Ngoc Do, Yeonjeong Ha, Jung-Hwan Kwon. Leaching of microplastic-associated additives in aquatic environments: A critical review. Environmental Pollution 2022, 305 , 119258. https://doi.org/10.1016/j.envpol.2022.119258
  60. Zara L.R. Botterell, Melanie Bergmann, Nicole Hildebrandt, Thomas Krumpen, Michael Steinke, Richard C. Thompson, Penelope K. Lindeque. Microplastic ingestion in zooplankton from the Fram Strait in the Arctic. Science of The Total Environment 2022, 831 , 154886. https://doi.org/10.1016/j.scitotenv.2022.154886
  61. Qian Zhang, Yuan He, Runjing Cheng, Qian Li, Zhiyong Qian, Xiaohui Lin. Recent advances in toxicological research and potential health impact of microplastics and nanoplastics in vivo. Environmental Science and Pollution Research 2022, 29 (27) , 40415-40448. https://doi.org/10.1007/s11356-022-19745-3
  62. Dong Wang, Shaoguo Ru, Wei Zhang, Zhenzhong Zhang, Yuejiao Li, Lingchao Zhao, Lianxu Li, Jun Wang. Impacts of nanoplastics on life-history traits of marine rotifer (Brachionus plicatilis) are recovered after being transferred to clean seawater. Environmental Science and Pollution Research 2022, 29 (28) , 42780-42791. https://doi.org/10.1007/s11356-021-18121-x
  63. Kunsheng Hu, Yangyang Yang, Jian Zuo, Wenjie Tian, Yuxian Wang, Xiaoguang Duan, Shaobin Wang. Emerging microplastics in the environment: Properties, distributions, and impacts. Chemosphere 2022, 297 , 134118. https://doi.org/10.1016/j.chemosphere.2022.134118
  64. Dongmei Xie, Hui Wei, Jae-Seong Lee, Minghua Wang. Mercury can be transported into marine copepod by polystyrene nanoplastics but is not bioaccumulated: An increased risk?. Environmental Pollution 2022, 303 , 119170. https://doi.org/10.1016/j.envpol.2022.119170
  65. Jérémy Thery, Capucine Bialais, Maria Kazour, Myriam Moreau, Dylan Dufour, Samira Benali, Rachid Amara, Sébastien Monchy, Jean-Marie Raquez, Sami Souissi. A New Method for Microplastics Identification in Copepods. Frontiers in Environmental Chemistry 2022, 3 https://doi.org/10.3389/fenvc.2022.905303
  66. João Vitor Fonseca da Silva, Fernando Miranda Lansac-Tôha, Bianca Trevizan Segovia, Felipe Emiliano Amadeo, Louizi de Souza Magalhães Braghin, Luiz Felipe Machado Velho, Hugo Sarmento, Claudia Costa Bonecker. Experimental evaluation of microplastic consumption by using a size-fractionation approach in the planktonic communities. Science of The Total Environment 2022, 821 , 153045. https://doi.org/10.1016/j.scitotenv.2022.153045
  67. Ya-Qi Zhang, Marianna Lykaki, Marta Markiewicz, Mohammad Taher Alrajoula, Caroline Kraas, Stefan Stolte. Environmental contamination by microplastics originating from textiles: Emission, transport, fate and toxicity. Journal of Hazardous Materials 2022, 430 , 128453. https://doi.org/10.1016/j.jhazmat.2022.128453
  68. Minling Gao, Linsen Bai, Xitong Li, Shengli Wang, Zhengguo Song. Combined effects of polystyrene nanoplastics on lead toxicity in dandelion seedlings. Environmental Pollution 2022, 76 , 119349. https://doi.org/10.1016/j.envpol.2022.119349
  69. Roland Geyer, Jenna Gavigan, Alexis M. Jackson, Vienna R. Saccomanno, Sangwon Suh, Mary G. Gleason. Quantity and fate of synthetic microfiber emissions from apparel washing in California and strategies for their reduction. Environmental Pollution 2022, 298 , 118835. https://doi.org/10.1016/j.envpol.2022.118835
  70. Ze Liu, Qian'en Huang, Hao Wang, Siyu Zhang. An enhanced risk assessment framework for microplastics occurring in the Westerscheldt estuary. Science of The Total Environment 2022, 817 , 153006. https://doi.org/10.1016/j.scitotenv.2022.153006
  71. Karli Sipps, Georgia Arbuckle-Keil, Robert Chant, Nicole Fahrenfeld, Lori Garzio, Kasey Walsh, Grace Saba. Pervasive occurrence of microplastics in Hudson-Raritan estuary zooplankton. Science of The Total Environment 2022, 817 , 152812. https://doi.org/10.1016/j.scitotenv.2021.152812
  72. Samantha N. Athey, Lisa M. Erdle. Are We Underestimating Anthropogenic Microfiber Pollution? A Critical Review of Occurrence, Methods, and Reporting. Environmental Toxicology and Chemistry 2022, 41 (4) , 822-837. https://doi.org/10.1002/etc.5173
  73. Christine M. Knauss, Christopher F. Dungan, Stuart A. Lehmann. A Paraffin Microtomy Method for Improved and Efficient Production of Standardized Plastic Microfibers. Environmental Toxicology and Chemistry 2022, 41 (4) , 944-953. https://doi.org/10.1002/etc.5216
  74. Gleyson B. Castro, Aline C. Bernegossi, Fernanda R. Pinheiro, Juliano J. Corbi. The silent harm of polyethylene microplastics: Invertebrates growth inhibition as a warning of the microplastic pollution in continental waters. Limnologica 2022, 93 , 125964. https://doi.org/10.1016/j.limno.2022.125964
  75. Vanesa Romero-Kutzner, Javier Tarí, Alicia Herrera, Ico Martínez, Daniel Bondyale-Juez, May Gómez. Ingestion of polyethylene microspheres occur only in presence of prey in the jellyfish Aurelia aurita. Marine Pollution Bulletin 2022, 175 , 113269. https://doi.org/10.1016/j.marpolbul.2021.113269
  76. Hongyou Wan, Junkai Wang, Xiaoyu Sheng, Jingwei Yan, Wei Zhang, Ying Xu. Removal of Polystyrene Microplastics from Aqueous Solution Using the Metal–Organic Framework Material of ZIF-67. Toxics 2022, 10 (2) , 70. https://doi.org/10.3390/toxics10020070
  77. Elma Lahive, Richard Cross, Aafke I. Saarloos, Alice A. Horton, Claus Svendsen, Rudolf Hufenus, Denise M. Mitrano. Earthworms ingest microplastic fibres and nanoplastics with effects on egestion rate and long-term retention. Science of The Total Environment 2022, 807 , 151022. https://doi.org/10.1016/j.scitotenv.2021.151022
  78. Iteb Boughattas, Nesrine Zitouni, Sabrine Hattab, Marouane Mkhinini, Omayma Missawi, Sondes Helaoui, Moncef Mokni, Noureddine Bousserrhine, Mohamed Banni. Interactive effects of environmental microplastics and 2,4-dichlorophenoxyacetic acid (2,4-D) on the earthworm Eisenia andrei. Journal of Hazardous Materials 2022, 424 , 127578. https://doi.org/10.1016/j.jhazmat.2021.127578
  79. Tânia Gomes, Agathe Bour, Claire Coutris, Ana Catarina Almeida, Inger Lise Bråte, Raoul Wolf, Michael S. Bank, Amy L. Lusher. Ecotoxicological Impacts of Micro- and Nanoplastics in Terrestrial and Aquatic Environments. 2022, 199-260. https://doi.org/10.1007/978-3-030-78627-4_7
  80. Giuseppe Bonanno. Fate, transport, and impact of microplastics on planktonic organisms. 2022, 75-94. https://doi.org/10.1016/B978-0-12-822471-7.00009-2
  81. Beatriz Pérez-Aragón, Juan Carlos Alvarez-Zeferino, Arely Areanely Cruz-Salas, Carolina Martínez-Salvador, Alethia Vázquez-Morillas. Ecotoxicity Assessment of Microplastics on Aquatic Life. 2022, 177-221. https://doi.org/10.1007/978-981-16-8440-1_9
  82. Krishna Gautam, Shreya Dwivedi, Sadasivam Anbumani. Microplastics in Biota. 2022, 355-376. https://doi.org/10.1007/978-3-030-39041-9_31
  83. Jun Wang, Xuan Li, Peng Li, Lianxu Li, Lingchao Zhao, Shaoguo Ru, Dahai Zhang. Porous microplastics enhance polychlorinated biphenyls-induced thyroid disruption in juvenile Japanese flounder (Paralichthys olivaceus). Marine Pollution Bulletin 2022, 174 , 113289. https://doi.org/10.1016/j.marpolbul.2021.113289
  84. Azim Haziq Zainuddin, Ahmad Zaharin Aris, Muhammad Rozaimi Mohd Zaki, Fatimah Md. Yusoff, Sze Yee Wee. Occurrence, potential sources and ecological risk estimation of microplastic towards coastal and estuarine zones in Malaysia. Marine Pollution Bulletin 2022, 174 , 113282. https://doi.org/10.1016/j.marpolbul.2021.113282
  85. Xiaoping Lang, Jie Ni, Zhen He. Effects of polystyrene microplastic on the growth and volatile halocarbons release of microalgae Phaeodactylum tricornutum. Marine Pollution Bulletin 2022, 174 , 113197. https://doi.org/10.1016/j.marpolbul.2021.113197
  86. Jin Il Kwak, Huanliang Liu, Dayong Wang, Young Hwan Lee, Jae-Seong Lee, Youn-Joo An. Critical review of environmental impacts of microfibers in different environmental matrices. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 2022, 251 , 109196. https://doi.org/10.1016/j.cbpc.2021.109196
  87. Feng Zhang, Guyu Peng, Pei Xu, Lixin Zhu, Changjun Li, Nian Wei, Daoji Li. Ecological risk assessment of marine microplastics using the analytic hierarchy process: A case study in the Yangtze River Estuary and adjacent marine areas. Journal of Hazardous Materials 2021, 12 , 127960. https://doi.org/10.1016/j.jhazmat.2021.127960
  88. Amy L. Lusher, Rachel Hurley, Hans Peter H. Arp, Andy M. Booth, Inger Lise N. Bråte, Geir W. Gabrielsen, Alessio Gomiero, Tânia Gomes, Bjørn Einar Grøsvik, Norman Green, Marte Haave, Ingeborg G. Hallanger, Claudia Halsband, Dorte Herzke, Erik J. Joner, Tanja Kögel, Kirsten Rakkestad, Sissel B. Ranneklev, Martin Wagner, Marianne Olsen. Moving forward in microplastic research: A Norwegian perspective. Environment International 2021, 157 , 106794. https://doi.org/10.1016/j.envint.2021.106794
  89. Juthamas Phothakwanpracha, Thaithaworn Lirdwitayaprasit, Supanut Pairohakul. Effects of sizes and concentrations of different types of microplastics on bioaccumulation and lethality rate in the green mussel, Perna viridis. Marine Pollution Bulletin 2021, 173 , 112954. https://doi.org/10.1016/j.marpolbul.2021.112954
  90. Jinyoung Song, Joorim Na, Dahee An, Jinho Jung. Role of benzophenone-3 additive in chronic toxicity of polyethylene microplastic fragments to Daphnia magna. Science of The Total Environment 2021, 800 , 149638. https://doi.org/10.1016/j.scitotenv.2021.149638
  91. Harriet L. Paterson, Jessica L. Stead, Thomas Crutchett, Renae K. Hovey, Benjamin M. Ford, Peter Speldewinde, Lina M. Zapata-Restrepo, Lu Yanfang, Xiaoyu Zhang, Andrew B. Cundy. Battling the known unknowns: a synoptic review of aquatic plastics research from Australia, the United Kingdom and China. Environmental Science: Processes & Impacts 2021, 23 (11) , 1663-1680. https://doi.org/10.1039/D1EM00175B
  92. Ning Gao, Zhihui Huang, Jianing Xing, Siyi Zhang, Jing Hou. Impact and Molecular Mechanism of Microplastics on Zebrafish in the Presence and Absence of Copper Nanoparticles. Frontiers in Marine Science 2021, 8 https://doi.org/10.3389/fmars.2021.762530
  93. Penelope K. Lindeque, Zara L. R. Botterell, Rachel L. Coppock, Matthew Cole. Plastics and Plankton in Our Seas. Frontiers for Young Minds 2021, 9 https://doi.org/10.3389/frym.2021.588638
  94. Huirong Yang, Yinglin He, Yumeng Yan, Muhammad Junaid, Jun Wang. Characteristics, Toxic Effects, and Analytical Methods of Microplastics in the Atmosphere. Nanomaterials 2021, 11 (10) , 2747. https://doi.org/10.3390/nano11102747
  95. Zakaria Daoud Taha, Roswati Md Amin, Sabiqah Tuan Anuar, Ammar Arif Abdul Nasser, Erqa Shazira Sohaimi. Microplastics in seawater and zooplankton: A case study from Terengganu estuary and offshore waters, Malaysia. Science of The Total Environment 2021, 786 , 147466. https://doi.org/10.1016/j.scitotenv.2021.147466
  96. Emily A. Shore, James A. deMayo, Melissa H. Pespeni. Microplastics reduce net population growth and fecal pellet sinking rates for the marine copepod, Acartia tonsa. Environmental Pollution 2021, 284 , 117379. https://doi.org/10.1016/j.envpol.2021.117379
  97. Sabrina M. Rodrigues, Michael Elliott, C. Marisa R. Almeida, Sandra Ramos. Microplastics and plankton: Knowledge from laboratory and field studies to distinguish contamination from pollution. Journal of Hazardous Materials 2021, 417 , 126057. https://doi.org/10.1016/j.jhazmat.2021.126057
  98. Ya-Qi Zhang, Marianna Lykaki, Mohammad Taher Alrajoula, Marta Markiewicz, Caroline Kraas, Sabrina Kolbe, Kristina Klinkhammer, Maike Rabe, Robert Klauer, Ellen Bendt, Stefan Stolte. Microplastics from textile origin – emission and reduction measures. Green Chemistry 2021, 23 (15) , 5247-5271. https://doi.org/10.1039/D1GC01589C
  99. Samira G. M. Portugal, Carlos A. B. Oses, Mariana G. R. Thiago, Christina W. C. Branco. Uptake of Microplastics by a Tropical Freshwater Cladocera Revealed by Polyethylene Terephthalate Fluorescence. Water, Air, & Soil Pollution 2021, 232 (8) https://doi.org/10.1007/s11270-021-05291-0
  100. Zhuoan Bai, Nan Wang, Minghua Wang. Effects of microplastics on marine copepods. Ecotoxicology and Environmental Safety 2021, 217 , 112243. https://doi.org/10.1016/j.ecoenv.2021.112243
Load all citations
  • Abstract

    Figure 1

    Figure 1. Ingestion and egestion of microplastics by juvenile Calanus finmarchicus: (A) nylon fibers (10 × 30 μm) in the intestinal tract; (B) nylon granules (10–30 μm) in the faecal pellets. Nylon microplastics were fluorescently dyed with Nile Red and visualized under stereo microscope (Leica MZAPO/Nikon DigitalSight Fi1-U2) equipped with a Leica “green” fluorescent filter (excitation 546/10 nm, dichroic splitter 565 nm and emission OG590). Yellow bars: 100 μm.

    Figure 2

    Figure 2. Juvenile Calanus finmarchicus ingestion rates (μg C individual–1 day–1) for: (A) D. tertiolecta; (B) T. rotula; (C) S. trochoidea; and (D) total algae. Results displayed as mean with standard error. * denotes significant different from control (P < 0.05).

    Figure 3

    Figure 3. Impact of fibrous and particulate microplastics on lipid accumulation in C. finmarchicus. The lipid mass (μg) of juvenile (CV), female and male C. finmarchicus prior to the start of experiment (Tzero; checked pattern) and following a 6-day exposure period. Treatments: control (white), nylon fibers (light gray), and nylon granules (dark gray). Letters show significant difference between treatments (ANOVA with posthoc Tukey).

    Figure 4

    Figure 4. Impact of fibrous and particulate microplastics on moulting in C. finmarchicus. Percentage of copepods which moulted on each day of the exposure period. Treatments: control (white), nylon fibers (light gray), and nylon granules (dark gray). Letters denote significant difference (in moulting each day) between treatments (P < 0.05).

  • References

    ARTICLE SECTIONS
    Jump To

    This article references 69 other publications.

    1. 1
      Hartmann, N. B.; Hüffer, T.; Thompson, R.; Hassellöv, M.; Verschoor, A.; Daugaard, A.; Rist, S.; Karlsson, T. M.; Brennholt, N.; Cole, M.; Herrling, M.; Heß, M.; Ivleva, N.; Lusher, A.; Wagner, M. Are we speaking the same language? Recommendations for a definition and categorization framework for plastic debris. Environ. Sci. Technol. 2019, 53, 10391047,  DOI: 10.1021/acs.est.8b05297
    2. 2
      Lusher, A. Microplastics in the marine environment: distribution, interactions and effects. In Marine Anthropogenic Litter; Bergmann, M., Gutow, L., Klages, M., Eds.; Springer: 2015; pp 245307.
    3. 3
      Cole, M.; Lindeque, P.; Halsband, C.; Galloway, T. S. Microplastics as contaminants in the marine environment: A review. Mar. Pollut. Bull. 2011, 62, 25882597,  DOI: 10.1016/j.marpolbul.2011.09.025
    4. 4
      Weinstein, J. E.; Crocker, B. K.; Gray, A. D. From macroplastic to microplastic: Degradation of high-density polyethylene, polypropylene, and polystyrene in a salt marsh habitat. Environ. Toxicol. Chem. 2016, 35 (7), 16321640,  DOI: 10.1002/etc.3432
    5. 5
      Eriksen, M.; Lebreton, L. C.; Carson, H. S.; Thiel, M.; Moore, C. J.; Borerro, J. C.; Galgani, F.; Ryan, P. G.; Reisser, J. Plastic Pollution in the World’s Oceans: More than 5 Trillion Plastic Pieces Weighing over 250,000 Tons Afloat at Sea. PLoS One 2014, 9 (12), e111913,  DOI: 10.1371/journal.pone.0111913
    6. 6
      Andrady, A. L. Persistence of plastic litter in the oceans. In Marine Anthropogenic Litter; Bergmann, M., Gutow, L., Klages, M., Eds.; Springer: 2015; pp 5772.
    7. 7
      FAO Microplastics in Fisheries and Aquaculture: Status of Knowledge on Their Occurrence and Implications for Aquatic Organisms and Food Safety; FAO: Rome, Italy, 2017; Vol. 615.
    8. 8
      Steer, M.; Cole, M.; Thompson, R. C.; Lindeque, P. K. Microplastic ingestion in fish larvae in the western English Channel. Environ. Pollut. 2017, 226, 250259,  DOI: 10.1016/j.envpol.2017.03.062
    9. 9
      Catarino, A. I.; Macchia, V.; Sanderson, W. G.; Thompson, R. C.; Henry, T. B. Low levels of microplastics (MP) in wild mussels indicate that MP ingestion by humans is minimal compared to exposure via household fibres fallout during a meal. Environ. Pollut. 2018, 237, 675684,  DOI: 10.1016/j.envpol.2018.02.069
    10. 10
      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 (15), 88188824,  DOI: 10.1021/es400931b
    11. 11
      Lusher, A.; McHugh, M.; Thompson, R. Occurrence of microplastics in the gastrointestinal tract of pelagic and demersal fish from the English Channel. Mar. Pollut. Bull. 2013, 67 (1–2), 9499,  DOI: 10.1016/j.marpolbul.2012.11.028
    12. 12
      Duncan, E. M.; Broderick, A. C.; Fuller, W. J.; Galloway, T. S.; Godfrey, M. H.; Hamann, M.; Limpus, C. J.; Lindeque, P. K.; Mayes, A. G.; Omeyer, L. C. Microplastic ingestion ubiquitous in marine turtles. Global change biology 2019, 25 (2), 744752,  DOI: 10.1111/gcb.14519
    13. 13
      Nelms, S.; Barnett, J.; Brownlow, A.; Davison, N.; Deaville, R.; Galloway, T.; Lindeque, P.; Santillo, D.; Godley, B. Microplastics in marine mammals stranded around the British coast: ubiquitous but transitory?. Sci. Rep. 2019, 9 (1), 1075,  DOI: 10.1038/s41598-018-37428-3
    14. 14
      Meeker, J. D.; Sathyanarayana, S.; Swan, S. H. Phthalates and other additives in plastics: human exposure and associated health outcomes. Philos. Trans. R. Soc., B 2009, 364 (1526), 20972113,  DOI: 10.1098/rstb.2008.0268
    15. 15
      Johansen, M. P.; Prentice, E.; Cresswell, T.; Howell, N. Initial data on adsorption of Cs and Sr to the surfaces of microplastics with biofilm. J. Environ. Radioact. 2018, 190, 130133,  DOI: 10.1016/j.jenvrad.2018.05.001
    16. 16
      Zuo, L.-Z.; Li, H.-X.; Lin, L.; Sun, Y.-X.; Diao, Z.-H.; Liu, S.; Zhang, Z.-Y.; Xu, X.-R. Sorption and desorption of phenanthrene on biodegradable poly (butylene adipate co-terephtalate) microplastics. Chemosphere 2019, 215, 2532,  DOI: 10.1016/j.chemosphere.2018.09.173
    17. 17
      Muller-Karanassos, C.; Turner, A.; Arundel, W.; Vance, T.; Lindeque, P. K.; Cole, M. Antifouling paint particles in intertidal estuarine sediments from southwest England and their ingestion by the harbour ragworm, Hediste diversicolor. Environ. Pollut. 2019, 249, 163170,  DOI: 10.1016/j.envpol.2019.03.009
    18. 18
      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 (23–24), 13691371,  DOI: 10.1080/15287394.2017.1385046
    19. 19
      Wright, S.; Rowe, D.; Thompson, R. C.; Galloway, T. S. Microplastic ingestion decreases energy reserves in marine worms. Curr. Biol. 2013, 23 (23), 10311033,  DOI: 10.1016/j.cub.2013.10.068
    20. 20
      Wegner, A.; Besseling, E.; Foekema, E.; Kamermans, P.; Koelmans, A. Effects of nanopolystyrene on the feeding behavior of the blue mussel (Mytilus edulis L.). Environ. Toxicol. Chem. 2012, 31 (11), 24902497,  DOI: 10.1002/etc.1984
    21. 21
      Besseling, E.; Wegner, A.; Foekema, E. M.; van den Heuvel-Greve, M. J.; Koelmans, A. A. Effects of Microplastic on Fitness and PCB Bioaccumulation by the Lugworm Arenicola marina (L.). Environ. Sci. Technol. 2013, 47 (1), 593600,  DOI: 10.1021/es302763x
    22. 22
      Cole, M.; Lindeque, P.; Fileman, E.; Halsband, C.; Galloway, T. The impact of polystyrene microplastics on feeding, function and fecundity in the marine copepod Calanus helgolandicus. Environ. Sci. Technol. 2015, 49 (2), 11301137,  DOI: 10.1021/es504525u
    23. 23
      Sussarellu, R.; Suquet, M.; Thomas, Y.; Lambert, C.; Fabioux, C.; Pernet, M. E. J.; Le Goïc, N.; Quillien, V.; Mingant, C.; Epelboin, Y. Oyster reproduction is affected by exposure to polystyrene microplastics. Proc. Natl. Acad. Sci. U. S. A. 2016, 113 (9), 24302435,  DOI: 10.1073/pnas.1519019113
    24. 24
      Cole, M.; Lindeque, P. K.; Fileman, E.; Clark, J.; Lewis, C.; Halsband, C.; Galloway, T. S. Microplastics alter the properties and sinking rates of zooplankton faecal pellets. Environ. Sci. Technol. 2016, 50, 32393246,  DOI: 10.1021/acs.est.5b05905
    25. 25
      Galloway, T. S.; Cole, M.; Lewis, C. Interactions of microplastic debris throughout the marine ecosystem. Nature Ecology & Evolution 2017, 1 (5), s41559,  DOI: 10.1038/s41559-017-0116
    26. 26
      Irigoien, X.; Harris, R. P.; Verheye, H. M.; Joly, P.; Runge, J.; Starr, M.; Pond, D.; Campbell, R.; Shreeve, R.; Ward, P. Copepod hatching success in marine ecosystems with high diatom concentrations. Nature 2002, 419 (6905), 387389,  DOI: 10.1038/nature01055
    27. 27
      Cole, M.; Lindeque, P.; Fileman, E.; Halsband, C.; Goodhead, R.; Moger, J.; Galloway, T. S. Microplastic ingestion by zooplankton. Environ. Sci. Technol. 2013, 47 (12), 66466655,  DOI: 10.1021/es400663f
    28. 28
      Setälä, O.; Fleming-Lehtinen, V.; Lehtiniemi, M. Ingestion and transfer of microplastics in the planktonic food web. Environ. Pollut. 2014, 185, 7783,  DOI: 10.1016/j.envpol.2013.10.013
    29. 29
      Lee, K.-W.; Shim, W. J.; Kwon, O. Y.; Kang, J.-H. Size-Dependent Effects of Micro Polystyrene Particles in the Marine Copepod Tigriopus japonicus. Environ. Sci. Technol. 2013, 47 (19), 1127811283,  DOI: 10.1021/es401932b
    30. 30
      Vroom, R. J.; Koelmans, A. A.; Besseling, E.; Halsband, C. Aging of microplastics promotes their ingestion by marine zooplankton. Environ. Pollut. 2017, 231, 987996,  DOI: 10.1016/j.envpol.2017.08.088
    31. 31
      Sun, X.; Li, Q.; Zhu, M.; Liang, J.; Zheng, S.; Zhao, Y. Ingestion of microplastics by natural zooplankton groups in the northern South China Sea. Mar. Pollut. Bull. 2017, 115 (1–2), 217224,  DOI: 10.1016/j.marpolbul.2016.12.004
    32. 32
      Desforges, J.-P. W.; Galbraith, M.; Ross, P. S. Ingestion of Microplastics by Zooplankton in the Northeast Pacific Ocean. Arch. Environ. Contam. Toxicol. 2015, 69 (4), 320330,  DOI: 10.1007/s00244-015-0172-5
    33. 33
      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 (11), 30743080,  DOI: 10.1002/etc.3881
    34. 34
      Botterell, Z. L.; Beaumont, N.; Dorrington, T.; Steinke, M.; Thompson, R. C.; Lindeque, P. K. Bioavailability and effects of microplastics on marine zooplankton: A review. Environ. Pollut. 2019, 245, 98110,  DOI: 10.1016/j.envpol.2018.10.065
    35. 35
      Paul-Pont, I.; Tallec, K.; Gonzalez-Fernandez, C.; Lambert, C.; Vincent, D.; Mazurais, D.; Zambonino-Infante, J.-L.; Brotons, G.; Lagarde, F.; Fabioux, C. Constraints and priorities for conducting experimental exposures of marine organisms to microplastics. Front. Mar. Sci. 2018, 5 (252) DOI: 10.3389/fmars.2018.00252 .
    36. 36
      Melle, W.; Runge, J.; Head, E.; Plourde, S.; Castellani, C.; Licandro, P.; Pierson, J.; Jonasdottir, S.; Johnson, C.; Broms, C. The North Atlantic Ocean as habitat for Calanus finmarchicus: Environmental factors and life history traits. Prog. Oceanogr. 2014, 129, 244284,  DOI: 10.1016/j.pocean.2014.04.026
    37. 37
      Pond, D. W. The physical properties of lipids and their role in controlling the distribution of zooplankton in the oceans. J. Plankton Res. 2012, 34 (6), 443453,  DOI: 10.1093/plankt/fbs027
    38. 38
      Marker, T.; Andreassen, P.; Arashkewich, E.; Hansen, B. W. Lipid deposition and sexual maturation in cohorts of Calanus finmarchicus (Gunnerus) originating from Bergen (60 N) and Tromsø (69 N) reared in Tromsø, Norway. Mar. Biol. 2003, 143 (2), 283296,  DOI: 10.1007/s00227-003-1089-5
    39. 39
      Lee, R. F.; Hagen, W.; Kattner, G. Lipid storage in marine zooplankton. Mar. Ecol.: Prog. Ser. 2006, 307, 273306,  DOI: 10.3354/meps307273
    40. 40
      Tarrant, A. M.; Baumgartner, M. F.; Hansen, B. H.; Altin, D.; Nordtug, T.; Olsen, A. J. Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus. Front. Zool. 2014, 11 (1), 91,  DOI: 10.1186/s12983-014-0091-8
    41. 41
      Jones, R. H.; Flynn, K. J.; Anderson, T. R. Effect of food quality on carbon and nitrogen growth efficiency in the copepod Acartia tonsa. Mar. Ecol.: Prog. Ser. 2002, 235, 147156,  DOI: 10.3354/meps235147
    42. 42
      Cole, M., Novel method for preparing microplastic fibres. Sci. Rep. 2016 DOI: 10.1038/srep34519 .
    43. 43
      Frost, B. W. Effect of size and concentration of food particles on the feeding behaviour of the marine planktoinic copepod Calanus pacificus. Limnol. Oceanogr. 1972, 17, 805815,  DOI: 10.4319/lo.1972.17.6.0805
    44. 44
      Folch, J.; Lees, M.; Sloane Stanley, G. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 1957, 226 (1), 497509
    45. 45
      R. C. Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2016.
    46. 46
      Meyer-Harms, B.; Irigoien, X.; Head, R.; Harris, R. Selective feeding on natural phytoplankton by Calanus finmarchicus before, during, and after the 1997 spring bloom in the Norwegian Sea. Limnol. Oceanogr. 1999, 44 (1), 154165,  DOI: 10.4319/lo.1999.44.1.0154
    47. 47
      Leiknes, Ø.; Striberny, A.; Tokle, N. E.; Olsen, Y.; Vadstein, O.; Sommer, U. Feeding selectivity of Calanus finmarchicus in the Trondheimsfjord. J. Sea Res. 2014, 85, 292299,  DOI: 10.1016/j.seares.2013.05.012
    48. 48
      Meyer, B.; Irigoien, X.; Graeve, M.; Head, R.; Harris, R. Feeding rates and selectivity among nauplii, copepodites and adult females of Calanus finmarchicus and Calanus helgolandicus. Helgoland Marine Research 2002, 56 (3), 169176,  DOI: 10.1007/s10152-002-0105-3
    49. 49
      Marshall, S.; Orr, A. On the biology of Calanus finmarchicus VIII. Food uptake, assimilation and excretion in adult and stage V Calanus. J. Mar. Biol. Assoc. U. K. 1955, 34 (3), 495529,  DOI: 10.1017/S0025315400008778
    50. 50
      Jemec, A.; Horvat, P.; Kunej, U.; Bele, M.; Kržan, A. Uptake and effects of microplastic textile fibers on freshwater crustacean Daphnia magna. Environ. Pollut. 2016, 219, 201209,  DOI: 10.1016/j.envpol.2016.10.037
    51. 51
      Bakir, A.; Rowland, S. J.; Thompson, R. C. Enhanced desorption of persistent organic pollutants from microplastics under simulated physiological conditions. Environ. Pollut. 2014, 185, 1623,  DOI: 10.1016/j.envpol.2013.10.007
    52. 52
      Litchman, E.; Ohman, M. D.; Kiørboe, T. Trait-based approaches to zooplankton communities. J. Plankton Res. 2013, 35 (3), 473484,  DOI: 10.1093/plankt/fbt019
    53. 53
      Blarer, P.; Burkhardt-Holm, P. Microplastics affect assimilation efficiency in the freshwater amphipod Gammarus fossarum. Environ. Sci. Pollut. Res. 2016, 23 (23), 2352223532,  DOI: 10.1007/s11356-016-7584-2
    54. 54
      Jónasdóttir, S. H. Lipid content of Calanus finmarchicus during overwintering in the Faroe–Shetland Channel. Fisheries Oceanography 1999, 8, 6172,  DOI: 10.1046/j.1365-2419.1999.00003.x
    55. 55
      Häfker, N. S.; Teschke, M.; Last, K. S.; Pond, D. W.; Hüppe, L.; Meyer, B. Calanus finmarchicus seasonal cycle and diapause in relation to gene expression, physiology, and endogenous clocks. Limnol. Oceanogr. 2018, 63 (6), 28152838,  DOI: 10.1002/lno.11011
    56. 56
      Crain, J. A.; Miller, C. B. Effects of starvation on intermolt development in Calanus finmarchicus copepodites: a comparison between theoretical models and field studies. Deep Sea Res., Part II 2001, 48 (1–3), 551566,  DOI: 10.1016/S0967-0645(00)00078-3
    57. 57
      Rodríguez, E. M.; Medesani, D. A.; Fingerman, M. Endocrine disruption in crustaceans due to pollutants: a review. Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol. 2007, 146 (4), 661671,  DOI: 10.1016/j.cbpa.2006.04.030
    58. 58
      Andersen, H. R.; Wollenberger, L.; Halling-Sørensen, B.; Kusk, K. O. Development of copepod nauplii to copepodites—a parameter for chronic toxicity including endocrine disruption. Environ. Toxicol. Chem. 2001, 20 (12), 28212829,  DOI: 10.1002/etc.5620201222
    59. 59
      Waddy, S.; Burridge, L.; Hamilton, M.; Mercer, S.; Aiken, D.; Haya, K. Rapid communication/communication rapide emamectin benzoate induces molting in American lobster, Homarus americanus. Can. J. Fish. Aquat. Sci. 2002, 59 (7), 10961099,  DOI: 10.1139/f02-106
    60. 60
      Guyon, A.; Smith, K. F.; Charry, M. P.; Champeau, O.; Tremblay, L. A. Effects of chronic exposure to benzophenone and diclofenac on DNA methylation levels and reproductive success in a marine copepod. J. Xenobiot. 2018, 8 (1), 7674,  DOI: 10.4081/xeno.2018.7674
    61. 61
      Jarry, H.; Christoffel, J.; Rimoldi, G.; Koch, L.; Wuttke, W. Multi-organic endocrine disrupting activity of the UV screen benzophenone 2 (BP2) in ovariectomized adult rats after 5 days treatment. Toxicology 2004, 205 (1–2), 8793,  DOI: 10.1016/j.tox.2004.06.040
    62. 62
      Kim, S.; Jung, D.; Kho, Y.; Choi, K. Effects of benzophenone-3 exposure on endocrine disruption and reproduction of Japanese medaka (Oryzias latipes)—A two generation exposure study. Aquat. Toxicol. 2014, 155, 244252,  DOI: 10.1016/j.aquatox.2014.07.004
    63. 63
      Kinnberg, K. L.; Petersen, G. I.; Albrektsen, M.; Minghlani, M.; Awad, S. M.; Holbech, B. F.; Green, J. W.; Bjerregaard, P.; Holbech, H. Endocrine-disrupting effect of the ultraviolet filter benzophenone-3 in zebrafish, Danio rerio. Environ. Toxicol. Chem. 2015, 34 (12), 28332840,  DOI: 10.1002/etc.3129
    64. 64
      Rochman, C. M.; Brookson, C.; Bikker, J.; Djuric, N.; Earn, A.; Bucci, K.; Athey, S.; Huntington, A.; McIlwraith, H.; Munno, K. Rethinking microplastics as a diverse contaminant suite. Environ. Toxicol. Chem. 2019, 38 (4), 703711,  DOI: 10.1002/etc.4371
    65. 65
      de Sá, L. C.; Oliveira, M.; Ribeiro, F.; Rocha, T. L.; Futter, M. N. Studies of the effects of microplastics on aquatic organisms: What do we know and where should we focus our efforts in the future?. Sci. Total Environ. 2018, 645, 10291039,  DOI: 10.1016/j.scitotenv.2018.07.207
    66. 66
      Lusher, A.; Welden, N.; Sobral, P.; Cole, M. Sampling, isolating and identifying microplastics ingested by fish and invertebrates. Anal. Methods 2017, 9, 13461360,  DOI: 10.1039/C6AY02415G
    67. 67
      Erni-Cassola, G.; Zadjelovic, V.; Gibson, M. I.; Christie-Oleza, J. A. Distribution of plastic polymer types in the marine environment; A meta-analysis. J. Hazard. Mater. 2019, 369, 691698,  DOI: 10.1016/j.jhazmat.2019.02.067
    68. 68
      Enders, K.; Lenz, R.; Stedmon, C. A.; Nielsen, T. G. Abundance, size and polymer composition of marine microplastics≥ 10 μm in the Atlantic Ocean and their modelled vertical distribution. Mar. Pollut. Bull. 2015, 100 (1), 7081,  DOI: 10.1016/j.marpolbul.2015.09.027
    69. 69
      Huvet, A.; Paul-Pont, I.; Fabioux, C.; Lambert, C.; Suquet, M.; Thomas, Y.; Robbens, J.; Soudant, P.; Sussarellu, R. Reply to Lenz et al.: Quantifying the smallest microplastics is the challenge for a comprehensive view of their environmental impacts. Proc. Natl. Acad. Sci. U. S. A. 2016, 113 (29), E4123E4124,  DOI: 10.1073/pnas.1607221113
  • Supporting Information

    Supporting Information

    ARTICLE SECTIONS
    Jump To

    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.9b01853.

    • Images of the microalgae, microplastics, and copepods; chemical data for the nylon fibers and granules; data relating to the size and shape of microalgae; and fatty acid and alcohol data for copepods in control, fiber, and granule treatments (PDF)


    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

Pair your accounts.

Export articles to Mendeley

Get article recommendations from ACS based on references in your Mendeley library.

Pair your accounts.

Export articles to Mendeley

Get article recommendations from ACS based on references in your Mendeley library.

You’ve supercharged your research process with ACS and Mendeley!

STEP 1:
Click to create an ACS ID

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

MENDELEY PAIRING EXPIRED
Your Mendeley pairing has expired. Please reconnect