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Article

Microplastics Residence Time in Marine Copepods: An Experimental Study

by
Saif Uddin
1,*,
Montaha Behbehani
1,
Nazima Habibi
1,*,
Scott W. Fowler
2,†,
Hanan A. Al-Sarawi
3 and
Carlos Alonso-Hernandez
4
1
Environment and Life Sciences Research Center, Kuwait Institute for Scientific Research, Safat 13109, Kuwait
2
School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, New York, NY 11794-5000, USA
3
Environment Public Authority, Shuwaikh Industrial 70050, Kuwait
4
Environmental Laboratories, International Atomic Energy Agency, 98000 Monaco, Monaco
*
Authors to whom correspondence should be addressed.
†
Present address: Institute Bobby, 8 Allée des Orangers, 06320 Cap d’Ail, France.
Sustainability 2023, 15(20), 14970; https://doi.org/10.3390/su152014970
Submission received: 29 August 2023 / Revised: 6 October 2023 / Accepted: 12 October 2023 / Published: 17 October 2023
(This article belongs to the Section Sustainable Oceans)
Browse Figure
Review Reports Versions Notes

Abstract

:
Microplastics are ubiquitous in aquatic environments, and in most marine environments, copepods are the main metazoans. The ingestion of microplastics by zooplankton is linked to various stresses, including oxidative stress, reduced reproductive capacities, and even mortality in nauplii. Microplastics are also reported to serve as vectors for hydrophobic contaminants. Our experimental results highlight that the retention and contact time of microplastics in copepods is quite short. The experimental results show that Parvocalanus crassirostis and Acartia pacifica defecated 75–84% and 61–71% of ingested microplastics within 60 min of ingestion. The observation raises several questions on the hypothesis of microplastic toxicity and ecological stresses: would a 180-minute contact time result in acute toxicity reported by various workers? An interesting observation was that these two copepod species did not consume microplastics larger than 50 µm in size. Considering this fact, inventories of smaller microplastics might be more important for assessing the ecological effects of MP ingestion among primary consumers in the marine food chain. Another important aspect that this study highlights is the likely change in faecal pellet sinking velocities due to the incorporation of MPs, and faecal pellets are probably efficient vectors for MP transport in the aquatic environment.

1. Introduction

Numerous publications have highlighted the ecological concern of microplastic (MP) ingestion in marine biota across the food chain from primary consumers to top predators. The ingested MP results in obstruction of the gastrointestinal tract and gills. The ingestion can also induce chemical toxicity due to the release of organic contaminants and metals used to manufacture polymers. Substantial evidence exists on MPs acting as vectors of contaminants as they provide a substrate for hydrophobic contaminants in aquatic environments [1,2,3,4,5,6,7,8].
A colossal quantity of microplastics (MPs) reaches the environment due to improper plastic waste disposal [9,10,11,12,13,14,15,16,17]. Studies have reported globally between 15 × 1012 and 51 × 1012 MPs float in the oceans [18,19,20,21,22,23]. Another estimate indicates that treated and untreated wastewater effluent contributes 1.47 × 1015 MPs y−1 and 3.85 × 1016 MPs y−1 respectively to worldwide aquatic habitats [14]. Substantial evidence exists that materials, from microbeads in detergents, cosmetic and personal care products, fibres from synthetic clothing [24,25,26,27], and micro rubber from tires [28], get into the aquatic environment from the discharge of waste streams, and from wet and dry depositions. The MPs remain in the water column for a long time before they accumulate in the bottom sediments [16] and are not available to pelagic organisms. Substantial evidence exists indicating that synthetic fibres account for over a third of MPs in the aquatic environment [29]. The ubiquitous presence, persistent nature, and capacity to act as a vector for hydrophobic pollutants in water as well as the potential to release harmful substances into aquatic habitats exacerbate MPs’ importance [17,30,31,32,33,34]. Both pelagic and benthic zones in aquatic systems are known to have plastic pollutants, with a reportedly negative effect on the ecology of these areas [17,35,36,37,38,39,40,41]. Publications report MP ingestion, accumulation and toxicity in a wide variety of marine biota [17,41]. The concern about MP ingestion emanates from the fact they can result in blockage of gills and digestive systems, malnutrition, and chemical toxicity due to the release of contaminants used for plastic manufacturing. The MPs tend to remain in the water column for a long time. During this time, they tend to degrade, resulting in the loss of loosely bound chemicals added to improve their properties. Microplastics are reported to contribute Bisphenol-A (BPA), Bisphenol-S (BPS), phthalates, and polybrominated diphenyl ethers (PBDEs) into aquatic environments [42]. The ecological effects of MPs are pronounced as they are likely to change reproductive behaviour and capacities; MP ingestion is also linked to malnutrition, hindering growth, inducing inflammation and oxidative stress [28,43,44,45,46,47,48,49,50].
There is a paucity of reliable data for a realistic understanding of MP ingestion; its likely effect on organism mortality and morbidity encouraged us to undertake this experimental study. Copepods are the most numerous mesozooplankton in the ocean [51,52,53], constituting about 70% of oceanic biomass [53]. Their omnipresence across the globe makes them a key component of the marine food chain [54,55]. Copepods form a significant link between primary producers and organisms at higher trophic levels, playing a vital role in marine nutrient cycling as the faecal pellets have high organic particulate content and high sinking velocities [56]. Laboratory studies have shown that MPs are ingested by copepods and egested in faecal pellets [57]. Parvocalanus crassirostis and Acartia pacifica have a sizeable spatial presence across the globe. These two species are relatively common in Persian Gulf waters. We have tried to understand if these organisms ingest MPs, whether they are translocated in different organs, and how long they are retained in the alimentary canal before being excreted.
Most of the ingestion studies have so far used virgin material and often a single shape, i.e., beads. We have tailored a unique approach that we consider more pragmatic; instead of commonly used virgin pellets in MP experiments, we have recovered MPs from the influent and sludge of a wastewater treatment plant (WWTP) since WWTPs are the largest source of MP input into the environment [14,15,22,58,59,60]. About 88–99.9% of the MPs in influent are trapped in sludge. Most of the recovered material is fibres, with some fragments as well. Usually, the MPs in sludge have undergone significant degradation and are likely similar in physico-chemical characteristics to those in the aquatic environment. We believe this type of material is more realistic for undertaking the toxicological assessment of MPs and for assessing their potential to act as vectors for hydrophobic contaminants.

2. Material and Methods

The large volume of seawater was sampled using the volume reduction method by using a 50 µm mesh size plankton net of 2 m length and 0.6 m diameter. Vertical trawls were used to collect samples from a 10 to 30 m depth in Kuwait waters between August 2020 and February 2021. The sampling locations were away from the coast (29°24′41″ N, 47°59′48″ E; 29°02′42″ N, 48°27′59″ E; 28°47′29″ N, 48°45′36″ E; 28°37′48″ N, 48°37′13″ E; 28°55′55″ N, 48°33′28″ E). All the samples collected on a single cruise day were transferred to filtered seawater. Samples were pooled together prior to identification at the lowest taxonomic level by a specialist using an identification guide [61]. Following the identification of copepods, monocultures were created. The stocking densities of 220 individuals L−1 for Parvocalanus crassirostis and 175 individuals L−1 for Acartia pacifica were maintained in a 50 L aquarium at 22 ± 0.5 °C temperature and 8.2 ± 0.1 pH. The aquariums were gently aerated, and a light:dark cycle of 16:8 h was maintained. Details are explained elsewhere [53].
In this experimental study, only the adult individuals of Acartia pacifica and Parvocalanus crassirostis were used. Three hundred adult copepods for each species were taken. To segregate the nauplii and faecal matter, the experiment was carried out in closed cascade cylindrical chambers with a mesh base; the first mesh was 90 µm in size, the second was 75 µm, and the third was 20 µm. The experimental setup was maintained at 22 ± 0.5 °C and the pH of the experimental tank was 8.2 ± 0.1 regulated using the IKS Aquastar system (IKS Aquaristik, Loessnitz, Germany). Prior to the addition of MPs, the copepods were kept for 3 h to allow for gut depuration. The design is described in detail elsewhere [62]. The fraction collected on 75 and 20 µm-sized sieves was moved into a smaller Petri dish to remove the nauplii, faecal pellets and detritus.
Microplastics were segregated from wastewater influent and sludge samples. These samples were collected in August 2020 from the Kabd wastewater treatment plant in Kuwait. The MP segregation and identification procedure is described in detail in our previous publications including the quality assurance and quality control measures [3,14,15,63,64,65]. For ease of readership, we have included the procedure briefly. A measure of 10 L wastewater from influent was collected in pre-cleaned 2 L amber glass bottles using a bailer. A stainless-steel shovel was used to collect about 1 kg of sludge sample in a pre-cleaned wide-mouth glass jar. Collected samples were brought to the microplastic laboratory at the Kuwait Institute for Scientific Research. The wastewater sample was added with 100 g of potassium hydroxide (Merck Schuchardt, Hohenbrunn, Germany) to oxidise the organic matter. The wastewater sample was kept at 40 °C for 48 h. The digested sample was vacuum filtered on a silver membrane filter of 0.45 µm pore size and 47 mm diameter (Sterlitech, Auburn, WA 98001, USA). The sample collected on the membrane was density-separated using a ZnCl2 (Merck Schuchardt, Hohenbrunn, Germany) saturated solution. The suspended material was isolated and transferred onto a coverslip (glass) and stained using Nile Red (10 μg mL−1 n-hexane). A measure of 1 mL of Nile Red solution was used and the glass coverslip was incubated for 30 min at 40 °C. For each extraction, 20 g of sewage sludge was taken and oxidised using 10 mL of 15% H2O2. Following the oxidation of organic matter, the sample was treated similarly to the wastewater.
For MP identification, a multi-tiered technique was used. Under a UV-stereomicroscope, the particles on the glass coverslip were evaluated for the existence of any cellular structure, consistency in diameter along the particle length with no bending or tapering, clarity, and no change in colour. Nile red also stains algae, black carbon, cellulose, chitin, cotton, natural waxes, paper goods, wood lignin, wool, and other OH-rich carbohydrates [66,67]. To ensure that they were not false positives, the hot needle method [4,38,68] was used. The extracted MPs were counted using an ultraviolet laser with a wavelength of 405 nm. MP particles were divided into three types: fibres, pieces, and films. In addition to physical identification, micro-Raman spectroscopy (-RAMAN) was used to characterize the polymers.
The MP polymer types were established by comparing the data in a polymer reference library (Supplementary File S1). The longest dimension of the MPs was measured using ImageJ software, and the shape and size of the MPs were also recorded. The most dominant form was fibre, and the most dominant polymers were polyester, polypropylene and polyacrylonitrile. Over 600 MPs with sizes ranging from 5 to 1000 µm were isolated (~600). Because of a priori knowledge of the smaller feed size preference of Acartia pacifica and Parvocalanus crassirostis, most of the isolated MPs were 50 µm and smaller. However, a few larger particles were also included in the experiment to test whether copepods consume them.
Contamination and carryover of MP from solvents and solutions were prevented by filtering all solutions with a 0.2 µm filter. All cleaned pieces of equipment were stored within a laminar flow hood and wrapped in aluminium foil. Along with the wastewater samples, negative controls of 10 L Millipore water were processed and analysed.
To retrieve the MPs after exposure, the faecal pellets and detrital material were collected and 15% H2O2 was added. The samples were kept at a constant temperature of 40 °C for at least 48 h. More than 15% H2O2 was added to samples that were not fully digested until a clear solution was obtained. The particles were removed from the digested sample using vacuum filtering using a 0.45 µm pore size and 47 mm diameter silver membrane filter (Sterlitech, Auburn, WA 98001, USA). The filtered material was density separated using a ZnCl2 (Merck Schuchardt, Hohenbrunn, Germany) saturated solution (density of 2.98 g cm3). Suspended material was carefully transferred onto a glass coverslip for counting under a microscope.

3. Results

One litre of filtered seawater was used for the ingestion experiment. A 0.2 µm membrane was used to filter the seawater and to ensure the removal of all MP. A measure of 10 mL of algal food consisting of Isocrysis gabana and Chaetoceros muelleri was added to the experimental tank. This algal food is well-suited for feeding the copepods. The feed concentration was approximately 1 × 106 cells/mL. In addition, 100 MPs of varying sizes from 5 to 1000 µm were added to a litre of filtered seawater. The experiment was repeated thrice for both Parvocalanus crassirostis and Acartia pacifica. In these experiments, the stocking density was 200 individuals L−1. The amount of algal feed ingested was variable, varying between 92 and 100% of that added. On three occasions, ingestion was less than <100% (Table 1). We realised that Parvocalanus crassirostis and Acartia pacifica ingested more particles in the less than 50 µm size range, while all the particles that were not ingested were >50 µm in size. This suggested that these copepod species might have a size preference for smaller MPs, similar to their prey size.
The result indicates that Parvocalanus crassirostis defecated 75–84% of ingested MPs within 60 min of ingestion, while 16–23% was ejected in 120 min, and only 2% was retained for 180 min (Figure 1). No MPs retained and remained in Parvocalanus crassirostis after 180 min., although we continued monitoring until 1440 min. since the samples were not analysed in real time. In the case of Acartia pacifica, 61–71% of ingested MPs was defecated in the first 60 min, whereas 27–38% was excreted within 120 min, and 1–2% of MPs was excreted within 180 min. Nevertheless, we continued our observation for a whole day, i.e., 1440 min, and did not observe any MPs. It is rather exciting and intriguing to note that there was a perfect mass balance; all the ingested MPs were excreted within 180 min.

3.1. Parvocalanus Crassirostris

The data were subjected to Shapiro–Wilk test. The data have a normal distribution at 60, 120 and 180 min (Table 2).
The Kruskal–Wallis H test indicated that there was a significant difference between the different groups, (χ2(2) = 7.26, p = 0.027). The mean rank score was 8 for MPs excreted in 60 min, 5 for MPs excreted in 120 min, and 2 for MPs excreted in 180 min. Dunn’s post hoc test returned a Bonferroni corrected alpha of 0.017 and indicated that the mean rank of the MPs pairs (x1–x3) was excreted in 60 min (x1) versus MPs excreted in 180 min (x3). The observed effect size η2 was 0.88. This indicates that the magnitude of the difference between the averages is large (Table 3).

3.2. Acartia Pacifica

The experimental data for Acartia pacifica was subjected to a Shapiro–Wilk test. The data have a normal distribution at 60, 120 and 180 min (Table 4).
In the case of Acartia pacifica, the Kruskal–Wallis (Table 5) H stats and Dunn’s post hoc test returned similar values. In this species, the observed effect size was large and the most significantly variable pair was MPs excreted in 60 min (x1) versus MPs excreted in 180 min (x3).
The excretion rates in the case of Parvocalanus crassirostis were 60 min > 120 min > 180 min and were found to be statistically significant with a p-value < 0.001. The pattern in the case of Acartia pacifica is similar with 60 min > 120 min > 180 min and is statistically significant. The Wilcoxson rank sum test was employed [69] to test the difference between the total number of MPs and the uptake of MPs. Thereafter, the Kruskal–Wallis test at a confidence level of 99.95% was conducted to investigate the difference between the average number of MPs excreted. The effect size was set at 0.3. Multiple comparisons were performed through Dunn’s post hoc test and the Bonferroni correction was applied to calculate an additional p value/2 or the false discovery rate [70].

4. Discussion

Many studies have indicated MP ingestion and various health effects among marine organisms [17,41,42,45,47,50,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93]. It can be a matter of serious concern when the small MPs in various shapes, sizes, and colours resembling prey are ingested as food not accidentally but preferentially. Microplastics have been reported in multiple groups, including copepods, fish, and crustaceans [94]. Many of these indicate oxidative stress, impaired reproductive capacities, and malnutrition. Most of the laboratory studies have used virgin plastic and beads of different sizes, and they have often been working with non-environmental concentrations that are several orders of magnitude higher than actual MP concentrations of 0.001–100 MP/m3 in most marine waters. Some studies have shown polystyrene beads of 0.4 to 3.8 μm size translocated to appendages, including the antennules and urosome of the copepod Temora longicornis [74]. We are unsure how this could have been possible in an environmental sample since it is almost impossible to identify polymers in particles less than 1 µm, and the publications show an accumulation of 0.4 µm-sized polymers. In another study, MP ingestion in worms caused an energy deficit [76]. Some authors have demonstrated and claimed the trophic transfer of MPs. One study suggested that the abundance of smaller MPs can affect the chemosensory selectivity of zooplankton to select prey [95]. MPs are reported to have long-term retention of polystyrene particles with a diameter ranging from 7.3 to 30.6 µm in the alimentary canal of the copepod Centropages typicus [74]. The period of retention of polystyrene particles in the gut of zooplankton has reached seven days, although most of the natural food passes through within hours. In an interesting multigeneration experiment, copepods Tigriopus japonicus were fed polystyrene pellets of 0.05 μm, 0.5 μm, and 6 μm size; no mortality was observed in adults, but nauplii suffered mortality in the first generation [96]. There was no significant decrease in survival in the second generation. These results may imply that adverse effects in copepods are limited to juvenile copepods exposed to MPs.
Several laboratory and field studies have emphasised that MP ingestion is prevalent among marine copepods. The consequences of MP consumption include decreased feeding activity, reduced energy intake, and compromised growth and reproduction, leading to adverse population-level outcomes. There are reports that oxidative stress and energy depletion are vital mechanisms involved in the adverse effects of MPs on copepods, and transgenerational proteome plasticity may play a role in their resilience. It is reported that MPs can act as vectors for environmental contaminants in copepods, potentially increasing the bioavailability and hazards of toxicants in the marine ecosystem. However, the current understanding of the biological effects of microplastics in copepods is still limited. Many previous studies have focused on short-term exposure to high concentrations of virgin microbeads, reducing their findings’ ecological relevance since they are seldom found in the environment and at the concentrations used in these experiments.
Aged microplastics, which can leach out incorporated additives and exacerbate negative impacts, have been found to have more adverse effects on marine organisms. An elegant review on MP ingestion by copepods suggests [97] that there is a long way to go in establishing a comprehensive understanding of the ingestion. In our experimental setup, we saw that most of the MPs were defecated in 60 min and all of them within 180 min, raising concerns that such a short exposure/contact time would result in detrimental effects on the growth, induce toxicity, and probably result in mortality. Our observation can be linked to the possible reduction in the sinking rate of faecal pellets due to the incorporation of low-density MPs, and such observations have been reported previously by various workers for the Calanoid copepods Calanus helgolandicus and Centropages typicus [98,99], where the inclusion of polystyrene MPs has reduced the sinking velocity by 2.25 folds and can also obliterate the biogeochemical fluxes in the region of high MPs and copepod biomass. It should also be noted that polymers that are denser than seawater are likely to accelerate the vertical flux of faecal pellet transport. The data also suggest that MPs can be ingested by detrivores and organisms at higher trophic levels via faecal pellet consumption. The data underpin the hypothesis that faecal pellets are a vector for microplastics.

5. Conclusions

The results of this study show an uptake of MPs less than 50 µm size among both Parvocalanus crassirostis and Acartia pacifica. The consumption of smaller MPs at the bottom of the food chain by copepods highlights the need to have comprehensive MP inventories of smaller sizes that are often overlooked when using methodologies where 333 µm sampling gear is recommended for MP assessment in the water column. Contrary to the reports of long-term retention of MPs in the alimentary canal of the copepod, our experimental results show very quick clearance of MPs along with the faecal pellets through the digestive system. The issue of oxidative stress, toxicity and reproductive capacities is unlikely to result from such a brief exposure. The loading of 100 MPs in a litre of water was well above the natural background of most coastal waters and open seas, raising doubt on the likely ingestion of MPs by the calanoid copepods in the natural environment. However, our observation on defecation rates warrants more in-depth analyses and studies on the possible results of MP ingestion in the copepod population and the likelihood of food chain transfer. The quick ejection of MPs with faecal matter can obliterate the sinking velocities of faecal pellets and, in turn, the biogeochemical cycle in the areas with high MP inventories and copepod populations. Since copepods are the most numerous metazoans amounting to almost 70% of the oceanic biomass, they can play a crucial role in MP redistribution via sinking faecal pellets. The ingestion of MP-laden faecal pellets by detrivores can be a mechanism of effective MP transfer in the marine food chain. The sinking velocity of faecal pellets can be reduced by the incorporation of low-density MPs while it can be accelerated if higher-density MPs are ingested. The data highlight the need to undertake ecological assessments of microplastics in the marine environment.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/su152014970/s1, The supplementary material includes Supplementary File S1: Microplastic reference spectra.

Author Contributions

Conceptualisation, S.U.; methodology, S.U., M.B. and C.A.-H.; software, N.H.; validation, M.B., S.W.F., H.A.A.-S. and S.U.; formal analysis, S.U. and M.B.; investigation, S.U., M.B. and N.H.; resources, H.A.A.-S. and C.A.-H.; data curation, M.B. and N.H.; writing original draft preparation, S.U., S.W.F. and C.A.-H.; writing review and editing, S.U.; visualisation, S.U. and N.H.; supervision, S.U.; project administration, S.U., N.H. and M.B.; funding acquisition, S.U. All authors have read and agreed to the published version of the manuscript.

Funding

The following funding sources are acknowledged: 1. Kuwait Institute for Scientific Research: EM092C; 2. Kuwait Foundation for the Advancement of Sciences: Grant No. PN18-14SC-01; International Atomic Energy Agency: Project RAS7038.

Institutional Review Board Statement

Ethical review and approval are not required for this study.

Informed Consent Statement

Not applicable as no humans were involved.

Data Availability Statement

The data are available in a Supplementary File and as part of the Kuwait Institute for Scientific Research Progress Report for RAS7038, which can be made available on request.

Acknowledgments

We are thankful to the Kuwait Institute for Scientific Research for supporting project EM092C and to the Kuwait Foundation for Advancement of Sciences, grant no PN18-14SC-01 for supporting a related study. Thanks are due to the International Atomic Energy Agency for supporting the project RAS7038 “Monitoring of the Marine Environment for Enhanced Understanding of the Abundance and Impact of Marine Plastic Pollution in Asia and the Pacific”.

Conflicts of Interest

The authors declare no conflict of interest.

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Sustainability 15 14970 g001
Figure 1. Microplastic ejection rates in two Calanoid Copepods, Parvocalanus crassirostis and Acartia pacifica.
Figure 1. Microplastic ejection rates in two Calanoid Copepods, Parvocalanus crassirostis and Acartia pacifica.
Sustainability 15 14970 g001
Table 1. The number of microplastics ingested and excreted by Parvocalanus crassirostis and Acartia pacifica at different time intervals.
Table 1. The number of microplastics ingested and excreted by Parvocalanus crassirostis and Acartia pacifica at different time intervals.
SampleNo. of MPs AddedNo. of MPs IngestedNo. of MPs Excreted
60 min120 min180 min1440 min
Experiment 1Parvocalanus crassirostis100927715--
Acartia pacifica10010061381-
Experiment 2Parvocalanus crassirostis1009773222-
Acartia pacifica1009870262-
Experiment 3Parvocalanus crassirostis1001008416--
Acartia pacifica10010069301-
Table 2. The Shapiro–Wilk test for Parvocalanus crassirostris.
Table 2. The Shapiro–Wilk test for Parvocalanus crassirostris.
Groups:60 min120 min180 min
Skewness:0.78221.59711.7321
Skewness Shape:Sustainability 15 14970 i001 Potentially Symmetrical (pval = 0.177)Sustainability 15 14970 i002 Potentially Symmetrical (pval = 0.445)Sustainability 15 14970 i003Potentially Symmetrical (pval = 0.157)
Excess kurtosis:NaNNaNNaN
Tails Shape:Sustainability 15 14970 i004Potentially Mesokurtic, normal like tails (pval = NaN)Sustainability 15 14970 i005Potentially Mesokurtic, normal like tails (pval = NaN)Sustainability 15 14970 i006Potentially Mesokurtic, normal like tails (pval = NaN)
Normality0.99860.43350.1305
Outliers:
Median:77160
Sample size (n):333
Rank sum (R):24156
R2/n:1927512
Table 3. The Kruskal–Wallis test in Parvocalanus crassirostris.
Table 3. The Kruskal–Wallis test in Parvocalanus crassirostris.
PairMean Rank DifferenceZSECritical Valuep-Valuep-Value/2
x1–x231.34732.22675.33060.17790.08895
x1–x362.69452.22675.33060.0070490.003524
x2–x331.34732.22675.33060.17790.08895
x1—MPs excreted in 60 min; x2—MPs excreted in 120 min; x3—MPs excreted in 180 min, Z—statistic parameter; SE—standard error, p-value—significance at the confidence level of 99.95% and p-value/2—adjusted false discovery rate after applying the Bonferroni correction.
Table 4. Shapiro–Wilk test for Acartia pacifica experimental data.
Table 4. Shapiro–Wilk test for Acartia pacifica experimental data.
Groups:60 min120 min180 min
Skewness:−1.65230.93521.7321
Skewness Shape:Sustainability 15 14970 i007Potentially Symmetrical (pval = 0.177)Sustainability 15 14970 i008Potentially Symmetrical (pval = 0.445)Sustainability 15 14970 i009Potentially Symmetrical (pval = 0.157)
Excess kurtosis:NaNNaNNaN
Tails Shape:Sustainability 15 14970 i010Potentially Mesokurtic, normal like tails (pval = NaN)Sustainability 15 14970 i011Potentially Mesokurtic, normal like tails (pval = NaN)Sustainability 15 14970 i012Potentially Mesokurtic, normal like tails (pval = NaN)
Normality0.33690.98950.1305
Outliers:
Median:69301
Sample size (n):333
Rank sum (R):24156
R2/n:1927512
Table 5. The Kruskal–Wallis test in Acartia pacifica.
Table 5. The Kruskal–Wallis test in Acartia pacifica.
PairMean Rank DifferenceZSECritical Valuep-Valuep-Value/2
x1–x231.34732.22675.33060.17790.08895
x1–x362.69452.22675.33060.0070490.003524
x2–x331.34732.22675.33060.17790.08895
x1—MPs excreted in 60 min; x2—MPs excreted in 120 min; x3—MPs excreted in 180 min, Z—statistic parameter; SE—standard error, p-value—significance at the confidence level of 99.95% and p-value/2—adjusted false discovery rate after applying the Bonferroni correction.
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Uddin, S.; Behbehani, M.; Habibi, N.; Fowler, S.W.; Al-Sarawi, H.A.; Alonso-Hernandez, C. Microplastics Residence Time in Marine Copepods: An Experimental Study. Sustainability 2023, 15, 14970. https://doi.org/10.3390/su152014970

AMA Style

Uddin S, Behbehani M, Habibi N, Fowler SW, Al-Sarawi HA, Alonso-Hernandez C. Microplastics Residence Time in Marine Copepods: An Experimental Study. Sustainability. 2023; 15(20):14970. https://doi.org/10.3390/su152014970

Chicago/Turabian Style

Uddin, Saif, Montaha Behbehani, Nazima Habibi, Scott W. Fowler, Hanan A. Al-Sarawi, and Carlos Alonso-Hernandez. 2023. "Microplastics Residence Time in Marine Copepods: An Experimental Study" Sustainability 15, no. 20: 14970. https://doi.org/10.3390/su152014970

APA Style

Uddin, S., Behbehani, M., Habibi, N., Fowler, S. W., Al-Sarawi, H. A., & Alonso-Hernandez, C. (2023). Microplastics Residence Time in Marine Copepods: An Experimental Study. Sustainability, 15(20), 14970. https://doi.org/10.3390/su152014970

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