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Influence of polystyrene microplastics on the growth, photosynthetic efficiency and aggregation of freshwater microalgae Chlamydomonas reinhardtii

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... The SEM images indicate that the surface of MBGS seemed to become more wrinkled with an increasing concentration of nPET. It was also reported that MPs could wrap around the surface of microalgae according to the SEM images [38]. Therefore, it can be speculated that high concentrations of nPET increase the production of EPS, which in turn allows more nPET encapsulated on the surface of MBGS to be adsorbed, further affecting the physiological activity of MBGS. Figure 3b suggests that MBGS might stimulate the production of more Chl to maintain overall photosynthesis and better adapt to highly turbid water. ...
... The SEM images indicate that the surface of MBGS seemed to become more wrinkled with an increasing concentration of nPET. It was also reported that MPs could wrap around the surface of microalgae according to the SEM images [38]. Therefore, it can be speculated that high concentrations of nPET increase the production of EPS, which in turn allows more nPET encapsulated on the surface of MBGS to be adsorbed, further affecting the physiological activity of MBGS. ...
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The widely used plastics in our daily lives have resulted in ubiquitous microplastics and nanoplastics in wastewater, such as polyethylene terephthalate (PET). As an emerging green process for wastewater treatment and resource recovery, microalgal–bacterial granular sludge (MBGS) aligns with the concept of the circular economy. However, it is unclear whether the tiny PET can affect the MBGS process. Thus, this study investigated the impact of nano–sized PET (nPET) on the MBGS process. The results showed that 10 to 30 mg/L nPET had no obvious impact on pollutant removal as compared with the control group. However, the performance of the MBGS with the addition of 50 mg/L nPET became worse after 15 days. Scanning electron microscopy revealed that the MBGS adsorbed nPET by generating extracellular polymeric substances. Further microbial analyses showed that the algal abundance in prokaryotes slowly declined with increasing concentrations of nPET, while the reduced energy storage and electron transfer in eukaryotes might lead to an inferior performance at 50 mg/L nPET. Overall, the MBGS was demonstrated to exhibit good adaptability to nPET–containing wastewater, which showed the potential to be applied for the treatment of municipal wastewater containing nanoplastics.
... The exposure of C. reinhardtii to increasing concentrations (5, 25, 50 and 100 mg L −1 ) of 300-600 nm PS resulted in decreased chlorophyll a fluorescence yields and photosynthetic activities. The PS beads adhered to the surface of microalgae, causing membrane damage [54]. Pd-doped PS-NPLs influenced the growth of both the filamentous cyanobacterium Anabaena sp. ...
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The present review critically examines the advancements in the past 5 years regarding research on the bioavailability and toxicity of the nanoplastics (NPLs) to freshwater plankton. We discuss the recent progress in the understanding of adsorption, absorption, trophic transfer, and biological effects in phyto- and zooplankton induced by NPLs exposure. The influence of plankton on NPLs’ bioavailability via the excretion of biomolecules and formation of eco-corona is also examined. Despite important research developments, there are still considerable knowledge gaps with respect to NPLs’ bioavailability and trophic transfer by plankton as well as a potential adverse effect in natural aquatic systems. As plankton play a critical role in primary production, nutrient cycling, and food web structure, understanding the interactions between NPLs and plankton is essential in assessing the potential implications of NPLs pollution for aquatic ecosystem biodiversity and services.
... Chlorophylls are related to the lightharvesting process, and the increase of pigments results in increasing photosynthetic rate (Falkowski and Raven 2013). In addition, the contents of soluble protein can be related to nutrient assimilation and be involved in osmoregulation (Li et al. 2020;Ma et al. 2021). Certain proteins (e.g. ...
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Different populations of the same species may have different physiological responses to environmental factors due to the adaptation to their environment. We tested interactive effects of temperatures (10,15, 20, 25, and 30 ℃) and nutrients (low nutrients: 5 μM NO3− and 0.5 μM PO4− (LN); medium nutrients: 50 μM NO3− and 5 μM PO4− (MN); high nutrients: 500 μM NO3− and 50 μM PO4− (HN)) in three different Ulva prolifera strains (one Chinese and two Korean strains). The results showed that all three strains of Ulva survived within the temperature range of 10 to 30 ℃. The photosynthetic rates of all strains increased with increasing temperature from 10 to 30 ℃ under MN. However, at the higher temperature (30 ℃) there was a significant reduction in the photosynthetic rate under HN in all three strains. A positive relationships between tissue nitrogen (N) and chlorophyll or soluble protein were observed in all three strains. The Chinese strain showed the lowest C:N ratio but the highest photosynthetic rate and tissue N contents. Our results show that the bloom forming Chinese strain may have higher nutrient uptake and assimilation ability, leading to higher photosynthetic activity. The Ulva strains may have lower tolerance to higher temperature at high nutrients conditions. These results suggest that the physiological responses of U. prolifera to different temperature and nutrients conditions can be population-specific.
... Plastics possess a protracted natural disintegration process, resulting in their enduring deposition within aquatic environments and soil for extended periods of time. Currently, the rising awareness of people (Cordier and Uehara 2019;Hu et al. 2019;Deng et al. 2020;Tong et al. 2020;Li et al. 2020;Anagnosti et al. 2021;Hu et al. 2022) has elucidated the effect of microplastic emissions and nano plastics on ecosystems and human health. New evidence suggests the presence of microplastic emissions in food along with the environment (Rochman et al. 2015;Yang et al. 2015;Karami et al. 2017;Gündoğdu et al. 2018) and water supplies (Pivokonsky et al. 2018;Mintenig et al. 2019) and our bodies. ...
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Plastic pollution has become a prominent and pressing environmental concern within the realm of pollution. In recent times, microplastics have entered our ecosystem, especially in freshwater. In the contemporary global landscape, there exists a mounting apprehension surrounding the manifold environmental and public health issues that have emerged as a result of the substantial accumulation of microplastics. The objective of the current study is to employ an enhanced grey prediction model in order to forecast global plastic production and microplastic emissions. This study compared the accuracy level of the four grey prediction models, namely, EGM (1,1, α, θ), DGM (1,1), EGM (1,1), and DGM (1,1, α) models, to evaluate the accuracy levels. As per the estimation of the study, DGM (1,1, α) was found to be more suitable with higher accuracy levels to predict microplastic emission. The EGM (1,1, α, θ) model has slightly better accuracy than the DGM (1,1, α) model in predicting global plastic production. Various accuracy measurement tools (MAPE and RMSE) were used to determine the model’s efficiency. There has been a gradual growth in both plastic production and microplastic emission. The current study using the DGM (1,1, α) model predicted that microplastic emission would be 1,084,018 by 2030. The present study aims to provide valuable insights for policymakers in formulating effective strategies to address the complex issues arising from the release of microplastics into the environment and the continuous production of plastic materials.
... The hetero-aggregation between Chlorella sp and pristine test groups and their mixtures was evaluated without shaking the culture at 6, 12, and 24 h, respectively, using the method described by Li et al. (2020a) and Yang et al. (2021). The supernatants were collected at a depth of 1 cm from the surface using a pipette, and the optical density (OD) was quantified at a wavelength of 680 nm using a UV spectrometer (Evolution 220, Thermo Fischer Scientific, USA). ...
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The ubiquitous presence of TiO2 nanoparticles (nTiO2) and microplastics (MPs) in marine ecosystems has raised serious concerns about their combined impact on marine biota. This study investigated the combined toxic effect of nTiO2 (1 mg/L) and NH2 and COOH surface functionalized polystyrene MPs (PSMPs) (2.5 and 10 mg/L) on Chlorella sp. All the experiments were carried out under both visible light and UV-A radiation conditions to elucidate the impact of light on the combined toxicity of these pollutants. Growth inhibition results indicated that pristine nTiO2 exhibited a more toxic effect (38%) under UV-A radiation when compared to visible light conditions (27%). However, no significant change in the growth inhibitory effects of pristine PSMPs was observed between visible light and UVA radiation conditions. The combined pollutants (nTiO2 + 10 mg/L PSMPs) under UV-A radiation exhibited more growth inhibition (nTiO2 + NH2 PSMPs 66%; nTiO2 + COOH PSMPs 50%) than under visible light conditions (nTiO2 + NH2 PSMPs 55%; TiO2 + COOH PSMPs 44%). Independent action modeling indicated that the mixture of nTiO2 with PSMPs (10 mg/L) exhibited an additive effect on the algal growth inhibition under both the light conditions. The photoactive nTiO2 promoted increased production of reactive oxygen species under UV-A exposure, resulting in cellular damage, lipid peroxidation, and impaired photosynthesis. The effects were more pronounced in case of the mixtures where PSMPs added to the oxidative stress. The toxic effects of the binary mixtures of nTiO2 and PSMPs were further confirmed through the field emission electron microscopy, revealing specific morphological abnormalities. This study provides valuable insights into the potential risks associated with the combination of nTiO2 and MPs in marine environments, considering the influence of environmentally relevant light conditions and the test medium.
... It provides important ecosystem services like sediment stabilisation, habitats providing for benthos and food providing for human beings (Reed et al., 2016;Gao et al., 2018a;Ou et al., 2023). Nevertheless, in the marine environment, MPs could be trapped by algae in four ways including twining, attachment, embedment and wrapping (Feng et al., 2020;Ng et al., 2022), which caused negative influences such as decreased photosynthetic rate, low specific growth rate and oxidative stress of algae (Li et al., 2020b;Liu et al., 2023;Xu et al., 2023). Moreover, MPs trapped by macroalgae could be transmitted into human via food web (Feng et al., 2020;Seng et al., 2020). ...
... High concentrations of electrolytes in natural colloids or suspensions promote heterogeneous aggregation of negatively charged NPs by reducing electrostatic repulsion Wu et al. 2022). Additionally, NPs form aggregates with microalgae and bacteria in the aquatic environment through polysaccharides secreted by cells (Li et al. 2020b;Pasqualini et al. 2023). The aggregation behavior of NPs in the aqueous environment is influenced by several factors. ...
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Environmental plastic wastes are continuously degraded into microplastics (MPs) and nanoplastics (NPs); the latter are more potentially harmful to organisms and human health as their smaller size and higher surface-to-volume ratio. Previous reviews on NPs mainly concentrate on specific aspects, such as sources, environmental behavior, and toxicological effects, but few focused on NPs-related scientific publications from a global point of view. Therefore, this bibliometric study aims to summarize the research themes and trends on NPs and also propose potential directions for future inquiry. Related papers were downloaded from the Web of Science Core Collection database on NPs published from 2008 to 2021, and then retrieved information was analyzed using CiteSpace 6.1 R2 and VOSviewer (version 1.6.). Research on NPs mainly involved environmental behaviors, toxicological effects, identification and extraction of NPs, whereas aquatic environments, especially marine systems, attracted more attentions from these scientists compare to terrestrial environments. Furthermore, the adsorption behavior of pollutants by NPs and the toxicological effects of organisms exposed to NPs are the present hotspots, while the regulation of humic acid (HA) on NPs behaviors and the environmental behavior of NPs in freshwater, like rivers and lakes, are the frontier areas of research. This study also explored the possible opportunities and challenges that may be faced in NPs research, which provide a valuable summary and outlook for ongoing NPs-related research, which may be of intrigue and noteworthiness for relevant researchers.
... Additionally, the MPs that enter into aquatic systems do not only potentially prevent phytoplankton photosynthetic processes from taking place, they can also directly harm phytoplankton (Cao, Sun et al. 2022). Previous studies have shown that increasing MP concentrations in the form of polystyrene (PS) can inhibit microalgal growth, reducing chlorophyll a production and photosynthetic activity (Li, Wang et al. 2020). Furthermore, phytoplankton aggregates can significantly affect MP transport from surface to deeper water layers in aqueous environments (Long, Moriceau et al. 2015). ...
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Hazards associated with microplastics (MPs) and the pollutants they absorb in freshwater lake ecosystems have become a hot research topic in academia. In this study, in order to investigate potential affiliated MP hazards, lake MP samples were collected from a typical subtropical freshwater lake system in China (Poyang Lake) during the dry season (here, you should show the specific months) to explore their potential toxic element (PTE) response (i.e., exposure to Cu, Pb, and Zn) respective to the ecological environment and resident phytoplankton. Results show that average MP abundance in surface water can reach up to 1800 items m−3, which higher in the Nanjishan Wetland National Nature Reserve (NWNNR) (1175 items m−3). Polyester (i.e., purified terephthalic acid [PTA]) and polyethylene (PE) were the main polymer types found in surface water, fiber was the main MP shape, and most of the MP particle sizes are greater than 100 μm. Moreover, phytoplankton biomass was significantly higher in the NWNNR compared to Poyang Lake’s retention basin and water channel. It indicated that MP pollutant status of Poyang Lake is mild; however, the ecological risks that MPs pose should not be ignored. The significant positive correlation between MPs and PTEs indicated that PTE absorption and desorption by MPs may cause potential ecological stress. Although we anticipate no direct link between ecotoxicity and phytoplankton, MPs may have indirect effects on phytoplankton through their regulatory effects on PTE levels in water.
... The damage of MPs on photosynthesis and oxidative stress in microalgae intensified with increasing concentrations. Many studies have also proved that microplastics have a concentration-dependent toxicity effect on microalgae (Wang et al., 2020a;Li et al., 2020). At high concentrations, the formation of heterogeneous aggregates may be responsible for the increased toxicity of MPs. ...
... It is well known that microbes associated with macroalgae often play a symbiotic and crucial part in macroalgal health, functioning, and development during the host's various life cycle stages (Ren et al., 2022). Direct damage and growth inhibition of the microorganisms due to exposure to MPs (Hazeem et al., 2020;Lanctôt et al., 2020;Li et al., 2020;Tamayo-Belda et al., 2023) and associated organic additives (i.e., phthalates, bisphenol A, and heavy metals) has been reported extensively in recent years. For example, exposure to MPs was correlated with cellular propagation and an overall development disorder of microorganisms (Qiu et al., 2022). ...
Article
Constantly raising microplastic (MP) contamination of water sources poses a direct threat to the gentle balance of the marine environment. This study focuses on a multifactor hazard evaluation of conventional (polyethylene - PE, polypropylene - PP, and polystyrene - PS) and alternative (polyethylene terephthalate with 25 % or 50 % recycled material and polylactic acid) plastics. The risk assessment framework explored included MP abundance, water acidification potential, surface oxidation, fragmentation, and bacterial growth inhibition. Based on MP monitoring campaigns worldwide, we conclude that PE-based plastics are the most abundant MPs in water samples (comprise up to 82 % the MP in those samples). A year-long weathering experiment showed that PS-based and PP-based plastics were oxidized to a higher extent, resulting in the highest water acidification with pH reduction of up to three orders of magnitude. Finally, our laboratory experiments showed that weathered PS was the most fragile plastic during mechanical degradation, while both PP- and PS-based plastic extracts showed a significant growth inhibition toward the marine microorganisms (Bacillus sp. and Pseudoaltermonas sp). Using the examined factors as weighted inputs into our framework, this holistic evaluation of hazards suggest that PP-based plastic products were the most hazardous compared to the other conventional and alternative plastic types.
... The hetero-aggregation between Chlorella sp and pristine test groups and their mixtures was evaluated without shaking the culture at 6, 12, and 24 h respectively using the method described by (Li et al. 2020a;Yang et al. 2021). The supernatants were collected at a depth of 1 cm from the surface using a pipette, and the optical density (OD) was quanti ed at a wavelength of 680 nm using a UV-spectrometer (Evolution 220, Thermo Fischer Scienti c, USA). ...
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The ubiquitous presence of TiO 2 nanoparticles (nTiO 2 ) and microplastics (MPs) in marine ecosystems has raised serious concerns about their combined impact on marine biota. In the natural environment, marine microalgae can interact with mixtures of nTiO 2 and MPs under both visible light and UV-A radiation conditions. However, most of the previous toxicity studies employed visible light conditions, so the influence of UV-A radiation on toxicity remains poorly understood. To address this gap, the current study aimed to compare the effects of visible light and UV-A radiation on the combined toxic effects of nTiO 2 and polystyrene microplastics (PSMPs) in the marine microalga Chlorella sp using artificial seawater directly as the test medium. Our results demonstrated that under UV-A radiation the algal growth inhibition was significantly enhanced compared to that in visible light conditions. The mixtures of nTiO 2 and PSMPs exhibited significant enhanced toxicity than their pristine forms. Specifically, the mixtures of nTiO 2 and NH 2 -functionalized PSMPs (10mg/L) showed higher toxicity to algae than the mixtures with COOH-functionalized PSMPs (10mg/L). Furthermore, UV-A radiation exacerbated the hetero aggregation between algae and pollutants. The photoactive nTiO 2 , promoted increased production of reactive oxygen species under UV-A exposure resulting in cellular damage, lipid peroxidation, and impaired photosynthesis. The effects were more pronounced in case of the mixtures where PSMPs added to the oxidative stress. The toxic effects of the binary mixtures of nTiO 2 and PSMPs were further confirmed through the Field Emission Electron Microscopy, revealing specific morphological abnormalities. This study provides valuable insights into the potential risks associated with the combination of nTiO 2 and MPs in marine environments, considering the influence of environmentally relevant light conditions and the test medium.
... The density of MPs is a preponderant factor in the distribution of these particles in water bodies (Borges-Ramírez et al. 2020). Therefore, MPs with lower density than water either float on the superficial layer or remain suspended in the water column with a neutral density, while denser MPs concentrate in the benthic environment (Li et al. 2020). Fish of benthic and benthopelagic habits in the Pomba River presented similar quantities of MPs (mean benthic =2.7 MPs; mean benthopelagic = 3.0 MPs), especially fibers. ...
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Pollution by synthetic polymers is even more problematic to the environment when this material is fragmented into small portions, forming microplastics (MPs). We analyzed the contamination of ichthyofauna by MPs in an important river of the Atlantic Rainforest in regard to abundance, diversity of morphotypes, polymers, colors, and sizes of the synthetic particles in 20 species of fish. Fish were collected in November 2019 and in March 2020 in five sites along the Pomba River. Of the 101 fish analyzed, 49 (49%) presented MPs in at least one organ. Of the 20 species of fish collected 13 included individuals with at least one MP in their analyzed organs. The organs, trophic categories and feeding areas did not affect the general abundance of MPs types. Blue MPs were predominant, followed by the colors black, red, and white. MP fibers represented 91% of total MPs. Most MPs were between 2 and 3 mm in size. Polyethylene terephthalate (PET), polypropylene (PP), polyamide (PA), polyvinylidene chloride “Nylon” (PVDC), and high-density polyethylene (HDPE) were detected in the fishes. The exposure of the fish species to MPs was associated mainly with individual size and species-specific aspects, regardless of ecological traits. Considering that 55% of the fish species studied are consumed by humans, it is necessary to study the potential impact of MP ingestion on human health and to understand to what extent we may be consuming both plastic particles and contaminants that are adsorbed to MPs.
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The pollution of microplastics (MPs) is a worldwide major concern, as they have become a major part of our food chain. MPs enter our ecosystem via different pathways, including anthropogenic activities and improper disposal of plastics. The aim of this article is to review the current scientific literature related to MPs and how they affect different life forms on earth. Briefly, MPs induced negative effects on humans are primarily linked with the oxidative stress and disruption in immunity. MPs not only affect the soil chemical and physical properties such as reduction in soil health and productivity but also impose harmful effects on soil microorganisms. Moreover, MP-induced plant growth reduction results from three complementary mechanisms: (i) reduction in root and shoot growth, (ii) reduction in photosynthesis accompanied by higher reactive oxygen species (ROS) production, and (iii) reduction in nutrient uptake via altered root growth. Given the negative effects of MPs on different life forms, it is important to remove or remediate them. We have discussed different MP removal methods including coagulation, membrane filtration technology, biochar, and biological degradation of MPs in soil and wastewater effluents. The use of ozone as ultrafiltration technique has also been shown as the most promising technique for MP removal. Finally, some future research recommendations are also put forward at the end to further enhance our understanding of the MPs induced negative effects on different life forms. Graphical abstract The flowchart shows the interaction of MPs from water contaminated with MPs with different parts of the ecosystem and final interaction with human health
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Background Microalgal biomass harvesting using traditional chemicals is costly for the production of biofuels, hindering the scale-up process of the technology. Thus, the search for a cost-effective microalgal harvesting method is extremely important. Using chitosan as a natural flocculant to harvest microalgal biomass seems to be an efficient and convenient solution. Although microalgal biomass flocculation by chitosan has been reported in some previous studies, literature on the harvesting of microalgae C. vulgaris biomass using such polymer is scanty. In addition, there is limited information available on whether the usage of chitosan during the harvesting will affect downstream lipid extraction. Still, whether microalgae can be re-grown with the spent medium after chitosan flocculation is still unknown. ResultsIn this study, microalgal biomass harvesting using chitosan as a natural flocculant and aluminum sulfate as a traditional flocculant was compared and evaluated. Optimal doses and effects on biomass sedimentation, spent medium recycling and lipid extraction were investigated. The results showed that the optimal doses for chitosan and aluminum sulfate to achieve more than 90% biomass recovery were 0.25 and 2.5 g/L, respectively. The sedimentation time of 10 min was found to be the most appropriate to remove over 90% biomass from culture. The spent medium after chitosan flocculation could be potentially recycled for the re-cultivation of microalgae, which demonstrated robust growth in comparison with those grown in the recycled medium from aluminum sulfate flocculation. The lipid content of microalgae harvested by chitosan reached 32.9, 4.6% higher than that of those harvested by aluminum sulfate, indicating that the application of the natural flocculant would not impact the downstream extraction of microalgal lipids. Conclusion The results herein presented, demonstrated that chitosan is applicable for microalgal harvesting during the upscaling process. Flocculation method developed by using chitosan as a natural flocculant is a worthy microalgal harvesting method for microalgae-based biofuel production. There is hope that chitosan can be reasonably and technically realistically applied in a full-scale process for the harvesting of microalgal biomass.
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Microplastics and pharmaceuticals are considered ubiquitous and emergent pollutants of high concern but the knowledge on their effects on primary producers is still limited, especially those caused by mixtures. Thus, the goal of the present study was to investigate if the presence of microplastics (1–5 μm diameter) influences the toxicity of the pharmaceuticals procainamide and doxycycline to the marine microalga Tetraselmis chuii. Bioassays (96 h) to investigate the toxicity of those substances individually and in mixtures (i.e. microplastics-procainamide mixtures and microplastics-doxycycline mixtures) were carried out. Effect criteria were the average specific growth rate (growth rate) and chlorophyll a concentration (chlorophyll). EC10, EC20 and EC50 were determined. Microplastics alone had no significant effects on growth rate up to 41.5 mg/l, whereas chlorophyll was significantly reduced at 0.9 and 2.1 mg/l of microplastics, but not at higher concentrations. The 96 h EC50 (growth rate and chlorophyll, respectively) determined for the other bioassays were: 104 and 143 mg/l for procainamide alone; 125 and 31 mg/l for procainamide in the presence of microplastics; 22 and 14 mg/l for doxycycline alone; 11 and 7 mg/l for doxycycline in the presence of microplastics. Significant differences (p < 0.001) between the toxicity curves of each pharmaceutical alone and in mixture with microplastics were found for procainamide (chlorophyll), and doxycycline (both parameters). Thus, both pharmaceuticals were toxic to T. chuii in the low ppm range, and microplastics-pharmaceutical mixtures were more toxic than the pharmaceuticals alone. Very high decreases of doxycycline concentrations in test media were found, indicating degradation of the antibiotic. Thus, although the biological results are expressed in relation to doxycycline concentration, the effects were likely caused by a mixture of the parental compound and its degradation products. The concentrations of microplastics and pharmaceuticals tested (low ppm range) are higher than those expected to be found in waters of the most part of marine ecosystems (ppt or ppb ranges). However, considering the widespread contamination by microplastics and pharmaceuticals, the concentrations already found in waters, sediments and/or organism of heavily polluted areas, the long-term exposure (over generations) of wild populations to such substances in polluted ecosystems and the possibilities of bioaccumulation and toxicological interactions, these findings are of concern and further research on microplastics-pharmaceuticals toxicological interactions is needed.
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Microalgae can effectively absorb nitrogen (N) and phosphorus (P) in wastewater, while growth characteristics can be affected by such nutrients. The influences of the N and P concentration on growth, biomass yield, protein yield, and cell ultrastructure of Chlamydomonas reinhardtii (C. reinhardtii) were investigated in this study. The results showed that, in the optimum conditions (24–72 mg/L for N and 4.5–13.5 mg/L for P), the final biomass and protein content of C. reinhardtii could reach maximum value, and the cell organelles (chloroplast, mitochondria,etc.) showed good structures with larger chloroplasts, and more and neater thylakoids. However, if the concentration of nutrients was much higher or lower than the optimal value, it would cause adverse effects on the growth of C. reinhardtii, especially in high nitrogen (1000 mg/L) and low phosphorus (0.5 mg/L) conditions. Under these extreme conditions, the ultrastructure of the cells was also damaged significantly as follows: the majority of the organelles were deformed, the chloroplast membrane became shrunken, and the mitochondria became swollen, even partial disintegrated (differing slightly under high-N and low-P conditions); furthermore, it is found that C. reinhardtii was more sensitive to low-P stress. On the basis of these results, our findings have general implications in the application of wastewater treatment.
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The toxicity and bioavailability of single arsenic species have been widely investigated, however, the biological effects of mixed arsenic species co-existing in natural waters still remain unknown. The objective of this work was to discern the adverse effects of combined arsenite (As(III)) and dimethylarsenic acid (DMA) on diatom Nitzschia palea. The combined ecotoxicity of As(III) and DMA on N. palea was observed to be time-dependent and showed dose-effect relation. The toxicity of DMA and As(III) mixture was higher than individual DMA or As(III) when the As(III) concentration was in the range of 0.085-0.316 mg L(-1). As the As(III) concentration increased from 0.487 to 0.858 mg L(-1), the antagonistic effect was found, which could be due to the higher thiols contents in the thiol-containing proteins (e.g., frustulins, silaffins and other glycoproteins). The content of malondialdehyde (MDA) in the treatment of mixed arsenic species was found to be at the same level compared to the As-free control after 72 h of exposure, indicating that the co-toxicity of As(III) and DMA on diatom frustules was not significant. Furthermore, the increase of frustule formation rate in the mixture of EC50 As(III)-EC10 DMA at 72 h exposure time indicated that the damaged diatom cell walls was likely repaired gradually. The results from this study suggested that the effects of co-existed arsenic species were concentration-specific and should be considered in the risk assessment of arsenic and development of water quality criteria for the protection of aquatic ecosystems.
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As part of the degradation process, it is believed that most plastic debris becomes brittle over time, fragmenting into progressively smaller particles. The smallest of these particles, known as microplastics, have been receiving increased attention due to the hazards they present to wildlife. To understand the process of plastic degradation in an intertidal salt marsh habitat, strips (15.2 × 2.5 cm) of high density polyethylene (HDPE), polypropylene (PP), and extruded polystyrene (PS) were field deployed in June 2014 and monitored for biological succession, weight, surface area, UV transmittance, and fragmentation. Subsets of strips were collected after 4, 8, 16, and 32 weeks. After 4 weeks, biofilm had developed on all three polymers with evidence of grazing periwinkles (Littoraria irrorata). The accreting biofilm resulted in an increased weight of the PP and PS strips at 32 weeks by 33.5 and 167.0%, respectively, with a concomitant decrease in UV transmittance by ∼99%. Beginning at 8 weeks, microplastic fragments and fibers were produced from strips of all three polymers, and scanning electron microscopy revealed surface erosion of the strips characterized by extensive cracking and pitting. The results of this study suggest that the degradation of plastic debris proceeds relatively quickly in salt marshes, and that surface delamination is the primary mechanism by which microplastic particles are produced in the early stages of degradation. This article is protected by copyright. All rights reserved.
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The amount of nano- and microplastic in the aquatic environment rises due to the industrial production of plastic and the degradation of plastic into smaller particles. Concerns have been raised about their incorporation into food webs. Little is known about the fate and effects of nanoplastic, especially for the freshwater environment. In this study, effects of nano polystyrene (Nano-PS) on the growth and photosynthesis of the green alga Scenedesmus obliquus and the growth, mortality, neonate production and malformations of the zooplankter Daphnia magna were assessed. Nano-PS reduced population growth and reduced chlorophyll concentrations in the algae. Exposed Daphnia showed a reduced body size and severe alterations in reproduction. Numbers and body size of neonates were lower, while the number of neonate malformations among neonates rose to 68% of the individuals. These effects of Nano-PS were observed between 0.22 and 103 mg Nano-PS/L. Malformations occurred from 30 mg Nano-PS/L onwards. Such plastic concentrations are much higher than presently reported for marine as well as freshwater, but may eventually occur in sediment pore waters. As far as we know, these results are the first to show that direct life history shifts in algae and Daphnia populations may occur as a result of exposure to nanoplastic.
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Microalgae cultures are receiving attention because of increasing biotechnological and biomedical production of active biomolecules. We evaluated various fertilizer-based culture media to scale up production of the marine microalga Phaeodactylum tricornutum for production of exocellular polysaccharides (EPS), soluble proteins, and cellular superoxide dismutase (SOD). The standard source of sodium nitrate was the same as that used in the synthetic f/2 culture medium and ammonium nitrate, urea, ammonium sulfate, and calcium nitrate as alternative sources of nitrogen. The maximum production of EPS was achieved in microalgae cells grown in the culture media containing 63 and 23% nitrogen from ammonium sulfate, and also in microalgae cells grown in the culture media containing 3% nitrogen from ammonium nitrate. The maximum production of cellular SOD was achieved in microalgae cells grown in the culture media containing 35 and 26% nitrogen from ammonium sulfate, and in the culture media containing 17% nitrogen from urea. The results suggest that it is possible to use a source of nitrogen, other than sodium nitrate, to scale up growth of P. tricornutum for production of EPS and SOD at reduced costs.
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mPVC inhibited the growth, chlorophyll content and photosynthetic efficiency of the algae. The physical blockage and aggregation were responsible for the inhibition.
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Silver nanomaterials (AgNMs) of different shapes and sizes are potentially toxic to aquatic organisms. However, studies on the toxicity of AgNMs and on their shape-dependent effects on algae are scarce. The present study evaluated the effects of three AgNMs (silver nanospheres, AgNPs; silver nanowires, AgNWs; silver nanoplates, AgPLs) with different shapes coated with polyvinylpyrrolidone on the growth and photosynthetic performance of an alga, Chlorococcum infusionum. We used growth measurements and determined the photosynthetic parameters based on chlorophyll fluorescence transients in the algal cells exposed to different concentrations of the three AgNMs. The effective concentrations at 50% (EC50) of AgNPs, AgNWs, and AgPLs were calculated to be 0.1, 0.045, and 0.021 mg/L, respectively. The results showed that the toxicity of AgNMs in C. infusionum was in the order, AgPLs (40 nm diameter) > AgNWs (21,000 nm length × 42 nm diameter) > AgNPs (57 nm diameter), based on the decrease in growth and three photosynthetic activities. We propose that the toxic potential of AgNMs is primarily dependent on their diameter and secondarily on their shape. Overall, this study provides, for the first time, a comparison of the growth and photosynthetic activities of C. infusionum exposed to AgNMs of three different shapes.
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Microplastics are a contaminant of emerging concern which enter the marine environment from a variety of sources. The ingestion and toxic effects of microplastics on marine life, especially for filter feeders, are a cause of concern in view of their ubiquitous nature and their similar size as food sources. To assess the toxic effects of microspheres ingested by brine shrimp larvae, we exposed Artemia parthenogenetica to 10 μm polystyrene microspheres at different concentrations. These concentrations were approximate to the extrapolated marine aquatic environmentally relevant concentrations. The lowest polystyrene concentrations at which ingestion was visualized in A. parthenogenetica were 12 ± 0.57 particles/mL (6.7 ± 0.32 μg/L) and 1.1 ± 0.16 particles/mL (0.61 ± 0.088 μg/L), respectively. There were no significant impacts on the survival, growth or development in A. parthenogenetica occurring over the 14-d exposure across a range of polystyrene nominal concentrations (1–1000 particles/mL or 0.55–550 μg/L). However, abnormal ultrastructures of intestinal epithelial cells were observed upon exposure to polystyrene microspheres, including fewer and disordered microvilli, an increased number of mitochondrion and the appearance of autophagosome. These phenomena could affect nutrition absorption and energy metabolism. Although no major acute or chronic toxicity effects on A. parthenogenetica were observed over 24-h or 14-d exposures, this study provides evidence that the ingestion of polystyrene microplastics at extrapolated environmentally relevant concentrations can be visualized through a microscope to be causing a series of responses in intestinal epithelial cells. Although no acute or chronic toxicity effects of ingested microplastics on Artemia were observed, they caused a series of responses in intestinal epithelial cells.
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The co-contamination discharge of Phthalate esters (PAEs) by human activities and the increased UV radiation is increasing in aquatic ecosystems. However, little information is available about the combined detrimental effects of UV and PAEs on phytoplankton. In this study, the combined effects of UV-B irradiation and di-(2-ethylhexyl) phthalate (DEHP) on photosynthesis and antioxidant system of Scenedesmus acuminatus, and the DEHP degradation were investigated. Results showed that UV-B radiation decreased the chlorophyll a fluorescence yield, photosynthetic activity (Fv/Fm), pigment content and superoxide dismutase activity. This radiation also increased the reactive oxygen species (ROS) production and soluble protein and malondialdehyde contents. UV-B radiation with 10 mg L-1 DEHP improved the Fv/Fm and alleviated the cell damage of S. acuminatus, and the addition of high DEHP concentration (≥50 mg L-1) aggravated cell damage. The ROS generation also decreased with the increased DEHP concentration. UV-B radiation can effectively promote the DEHP degradation, with the highest degradation rate of 89.9% at an initial DEHP concentration of 10 mg L-1 within 6 h. This result may be attributed to that UV-B irradiance induced DEHP degradation under the regulation of ROS generated by S. acuminatus. Our findings will contribute to the understanding of the combined toxic mechanisms of UV-B and DEHP and in the evaluation of ecological environment risks for primary producers in aquatic ecosystems.
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The rapid increase in plastic use over the last few decades has resulted in plastic pollution in freshwater and marine ecosystems. However, more attention has been paid to plastic pollution in marine ecosystems than to freshwater ecosystems. This research determined microplastic ingestion by Daphnia magna and the potential effect of microplastics on the organism's survival and reproduction. The study also examined the potential of microplastics to enhance algal growth in support of understanding effects of microplastic ingestion on the organism. When exposed to 25, 50, and 100mg/L fluorescent green polyethylene microbeads at size of 63-75μm, D. magna ingested significant amount of plastic microbeads. The number of ingested beads increased with increasing particle concentration and exposure time. However, no significant effect on survival and reproduction was observed although the gut of D. magna was filled with plastic microbeads. In the algal experiment, Raphidocelis subcapitata grew more in the exposure media with the present of plastic microbeads than without plastic microbeads. This result suggests that plastic microbeads could serve as substrates for R. subcapitata to grow. Raphidocelis subcapitata then could be transferred to the organism's gut and provided energy for survival and reproduction. Results of the present study add to the literature of microplastic ingestion by aquatic organisms. Caution should be taken when interpreting hazards of microplastics based on ingestion, such as the measurement unit and the presence of algae in the environment. Free access to the paper via this link https://authors.elsevier.com/a/1Wo16B8ccgY7h
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Microplastics and antimicrobials are widely spread environmental contaminants and more research on their toxicity is needed. The uptake and effects of the antimicrobial florfenicol, microplastics, and their mixtures on Corbicula fluminea were investigated. Bivalves were exposed for 96 h to florfenicol (1.8 and 7.1 mg/l), microplastics (0.2 and 0.7 mg/l), or mixtures of the two substances. After 96 h, all bivalves exposed to antimicrobial treatments had florfenicol in their body (e.g. 2 ± 1 μg/g). Microplastics were found in the gut, lumen of the digestive gland, connective tissue, hemolymphatic sinuses, and gills surface of animals. Florfenicol caused a significant inhibition of cholinesterase (ChE) activity (~ 32%). Animals exposed to 0.2 mg/l of microplastics showed ChE activity inhibition (31%), and no other significant alterations. Mixtures caused feeding inhibition (57–83%), significant ChE inhibition (44–57%) and of isocitrate dehydrogenase activity, and increased anti-oxidant enzymes activity and lipid peroxidation levels. Overall, the results indicate that C. fluminea take up florfenicol and microplastics from the water and accumulated or at least retained it in their body for some time; both florfenicol (low ppm range) and microplastics (ppb range) were toxic to C. fluminea, with mixtures containing florfenicol and microplastics being more toxic. Thus, the risk of exposure and toxic effects of florfenicol to C. fluminea and other bivalves, and its predators increase in ecosystems contaminated with the antimicrobial and microplastics, as well as to humans consuming contaminated species from these ecosystems.
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Phthalate esters (PAEs), a family of emerging environmental contaminants, have been frequently detected in soils and water. However, intensive studies on the toxicity of PAEs have focused on growth response of terrestrial and aquatic animals, while only limited attention has been paid to aquatic plants, especially phytoplankton, the primary producer in aquatic ecosystems. Therefore, the acute toxic effects and underlying mechanisms of dibutyl phthalate (DBP) at different concentrations (0-20mgL(-1)) on two typical freshwater algae (Scenedesmus obliquus and Chlorella pyrenoidosa) were investigated. The growth of S. obliquus and C. pyrenoidosa was conspicuously inhibited by DBP exposure at 2-20mgL(-1). The 96-h median effective concentration values (96h-EC50) were 15.3mgL(-1) and 3.14mgL(-1) for S. obliquus and C. pyrenoidosa, respectively, implying that the spherical C. pyrenoidosa is more sensitive to DBP than the spindle-shaped S. obliquus. As expected from the damage done to cell organelles (i.e. cell membranes, chloroplasts, and protein rings), cell densities and chlorophyll content conspicuously decreased under DBP treatments. Moreover, the algal growth inhibition was closely linked to the increased production of intracellular reactive oxygen species and malondialdehyde content, indicating oxidative stress and lipid peroxidation in both algae. This was proved by the increased activity of antioxidant enzymes such as superoxide dismutase and catalase. Our findings will contribute to the understanding of toxic mechanisms in PAEs and the evaluation of environmental risks for primary producers in aquatic ecosystems.
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The coupling of primary piggery wastewater as a culture medium with elevated CO2 aeration is thought to be an economically feasible option for the cultivation of microalgae. However, little information is available regarding the photosynthetic characteristics of microalgae and nutrient removal from wastewater at different CO2 concentrations. It was found that elevated CO2 aeration provided sustained growth at CO2 concentrations ranging from 5% to 15% and performed best with 5% CO2 aeration in primary piggery wastewater for Chlamydomonas reinhardtii growth. Photosynthesis, respiration, and nutrient uptake (total nitrogen and total phosphorus) were stimulated in response to CO2 enrichment, thus increasing nutrient uptake in primary piggery wastewater, particularly total nitrogen and total phosphorus. A study of carbon-concentrating mechanism-related gene expression revealed that the levels of mRNAs, such as CAH1, LCIB and HLA3, were significantly downregulated. This represents a possible method for the reconciliation of CO2-stimulated growth with mixotrophic cultivation of C. reinhardtii in diluted primary piggery wastewater.
Article
Microplastic (<5 mm) ingestion has been recorded in Galeus melastomus, the blackmouth catshark, around the Balearic Islands. In total 125 individuals were analyzed for microplastic ingestion. Results have shown that 16.80% of the specimens had ingested a mean value of 0.34 ± 0.07 microplastics/individual. Stomach fullness index ranged from 0.86 to 38.89% and regression analyses showed that fuller stomachs contained more microplastics. A higher quantity of filament type microplastics were identified compared to granular or hard plastic type. No significant differences were given between ingestion values of two locations over the continental shelf providing further evidence of the ubiquitous distribution of microplastics. The findings in this study reflect the availability of this man made contaminant to marine species in seafloor habitats. Based on results from this study, data on microplastic ingestion could be used to study trends in the amount and composition of litter ingested by marine animals in accordance with descriptor 10 of the Marine Strategy Framework Directive.
Article
To investigate toxic effects of microplastic on marine microalgae Skeletonema costatum, both algal growth inhibition test and non-contact shading test were carried out, and algal photosynthesis parameters were also determined. The SEM images were used to observe interactions between microplastic and algae. It was found that microplastic (mPVC, average diameter 1 μm) had obvious inhibition on growth of microalgae and the maximum growth inhibition ratio (IR) reached up to 39.7% after 96 h exposure. However, plastic debris (bPVC, average diameter 1 mm) had no effects on growth of microalgae. High concentration (50 mg/L) mPVC also had negative effects on algal photosynthesis since both chlorophyll content and photosynthetic efficiency (ΦPSⅡ) decreased under mPVC treatments. Shading effect was not one reason for toxicity of microplastic on algae in this study. Compared with non-contact shading effect, interactions between microplastic and microalage such as adsorption and aggregation were more reasonable explanations for toxic effects of microplastic on marine microalgae. The SEM images provided a more direct and reasonable method to observe the behaviors of microplastic.
Article
The aim of this work was to study the effect of tetracycline, which is on the growth, physiological characteristics, and contaminants removal by Chlamydomonas reinhardtii. The results showed that the biomass and photosynthetic pigment concentration of C. reinhardtii exposed to tetracycline were lower than those of the control, while the superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) activities, and the malondialdehyde (MDA) content, were higher than those of the control. Additionally, when the tetracycline concentration reached 0.25mg/L, the removal of total nitrogen (TN), total phosphorus (TP), and chemical oxygen demand (COD) decreased from 80.8 to 55.0%, 100 to 92.5%, and 36.5 to 11.5%, respectively. Thus, tetracycline concentrations of 0-0.25mg/L are expected to have a significant effect on the growth and nutrient removal of C. reinhardtii in recycled water from wastewater treatment plants.
Article
In comparison with marine environments, the occurrence of microplastics in freshwater environments is less understood. In the present study, we investigated microplastic pollution levels during 2015 in Taihu Lake, the third largest Chinese lake located in one of the most developed areas of China. The abundance of microplastics reached 0.01 × 106–6.8 × 106 items/km2 in plankton net samples, 3.4–25.8 items/L in surface water, 11.0–234.6 items/kg dw in sediments and 0.2–12.5 items/g ww in Asian clams (Corbicula fluminea). The average abundance of microplastics was the highest in plankton net samples from the southeast area of the lake and in the sediments from the northwest area of the lake. The northwest area of the lake was the most heavily contaminated area of the lake, as indicated by chlorophyll-α and total phosphorus. The microplastics were dominated by fiber, 100–1000 μm in size and cellophane in composition. To our best knowledge, the microplastic levels measured in plankton net samples collected from Taihu Lake were the highest found in freshwater lakes worldwide. The ratio of the microplastics in clams to each sediment sample ranged from 38 to 3810 and was negatively correlated to the microplastic level in sediments. In brief, our results strongly suggest that high levels of microplastics occurred not only in water but also in organisms in Taihu Lake.
Article
Polypropylene, low-density polyethylene, and high-density polyethylene pre-production plastic pellets were weathered for three years in three experimental treatments: dry/sunlight, seawater/sunlight, and seawater/darkness. Changes in chemical bond structures (hydroxyl, carbonyl groups and carbon-oxygen) with weathering were measured via Fourier Transform Infrared (FTIR) spectroscopy. These indices from experimentally weathered particles were compared to microplastic particles collected from oceanic surface waters in the California Current, the North Pacific Subtropical Gyre, and the transition region between the two, in order to estimate the exposure time of the oceanic plastics. Although chemical bonds exhibited some nonlinear changes with environmental exposure, they can potentially approximate the weathering time of some plastics, especially high-density polyethylene. The majority of the North Pacific Subtropical Gyre polyethylene particles we measured have inferred exposure times > 18 months, with some > 30 months. Inferred particle weathering times are consistent with ocean circulation models suggesting a long residence time in the open ocean.
Article
Microplastics, which are accumulating in marine sediments, are assumed to pose a risk for deposit feeding invertebrates. We tested whether the fiddler crab Uca rapax ingests and retains microplastics in its body. Furthermore, we investigated whether retention rates depend on (a) the quality of the marine environment in which the plastics were pre-weathered and on (b) their abundance. For this, polystyrene pellets were submersed at a polluted and a pristine site near Niterói, Brazil, for 2 weeks. Then specimens of U. rapax were, in laboratory experiments, exposed to fragments (180 - 250 μm) derived from these pellets for 2 months. After this period, microplastics were observed in the gills, stomach and hepatopancreas of the animals. However, fragment retention was not influenced by the two factors that we manipulated. The presence of microplastics in different organs of the crab supports the assumption that these particles have the potential to harm marine invertebrates.
Article
Marine filter feeders are exposed to microplastic because of their selection of small particles as food source. Baleen whales feed by filtering small particles from large water volumes. Macroplastic was found in baleen whales before. This study is the first to show the presence of microplastic in intestines of a baleen whale (Megaptera novaeangliae). Contents of its gastrointestinal tract were sieved, dissolved in 10% potassium hydroxide and washed. From the remaining dried material, potential synthetic polymer particles were selected based on density and appearance, and analysed by Fourier transform infrared (FTIR) spectroscopy. Several polymer types (polyethylene, polypropylene, polyvinylchloride, polyethylene terephthalate, nylon) were found, in varying particle shapes: sheets, fragments and threads with a size of 1mm to 17cm. This diversity in polymer types and particle shapes, can be interpreted as a representation of the varying characteristics of marine plastic and the unselective way of ingestion by M. novaeangliae. Copyright © 2015 Elsevier Ltd. All rights reserved.
Article
Effects of various concentrations (0.5, 1.0, 2.5, 5.0, 7.5, and 10.0mg/L) of lead (Pb(2+)) on the growth, bioaccumulation, and antioxidative defense system of green algae, Cladophora, was investigated. Low concentrations of Pb(2+) accelerated Cladophora growth, but concentrations of 10.0mg/L and above inhibited the growth because of the hinderance to photosynthesis. The total soluble sugar content of Cladophora was affected by Pb(2+) treatment, but the protein content showed no significant changes. The malondialdehyde (MDA) content and peroxidase(POD) activity of Cladophora gradually increased whereas superoxide dismutase(SOD) decreased with Pb(2+) concentrations. Catalase (CAT) activity exhibited no significant changes following Pb(2+) treatment. Pb(2+) accumulated in Cladophora and that the lead content in Cladophora was correlated with POD growth, MDA, and Metallothionein (MT). POD and MT play a role in the survival of Cladophora in Pb-contaminated environments. This study suggests that Cladophora can be a choice organism for the phytoremediation of Pb-polluted coastal areas. Copyright © 2014 Elsevier Inc. All rights reserved.
Article
Once believed to degrade into simple compounds, increasing evidence suggests plastics entering the environment are mechanically, photochemically and/or biologically degraded to the extent that they become imperceptible to the naked eye yet are not significantly reduced in total mass. Thus, more and smaller plastics particles, termed microplastics, reside in the environment and are now a contaminant category of concern. The current study tested the hypotheses that microplastics concentration would be higher in proximity to urban sources, and vary temporally in response to weather phenomena such as storm events. Triplicate surface water samples were collected approximately monthly between July and December 2011 from four estuarine tributaries within the Chesapeake Bay, USA using a manta net to capture appropriately sized microplastics (operationally defined as 0.3‒5.0 mm). Selected sites have watersheds with broadly divergent land use characteristics (e.g., proportion urban/suburban, agricultural and/or forested) and wide ranging population densities. Microplastics were found in all but one of 60 samples with concentrations ranging over three orders of magnitude (<1.0 to > 560 g/km(2)). Concentrations demonstrated statistically significant positive correlations with population density and proportion of urban/suburban development within watersheds. Greatest microplastics concentrations also occurred at three of four sites shortly after major rain events.
Article
Following use polymer materials may be released to the natural environment distributed to various environmental compartments and may undergo a variety of mechanical and chemical weathering processes. This study characterised the degradation of a latex polymer of different thicknesses under a range of environmental conditions in outdoor microcosms. Samples were immersed in either demineralised water, artificial freshwater and marine water media and exposed for a period of 200-250days with exposure starting at different times of the year. Effects of pH, agitation and the exclusion of light on degradation were also studied. At the end of the exposure period, recovery of polymer material≥1.6μm ranged from a low of 22.04% (±16.35, for the freshwater treatment at pH5.5) to a high of 97.73% (±0.38, for the exclusion of light treatment). The disappearance of the bulk material corresponded to an increase in nanoparticles and dissolved organic material in the test media. Modelled degradation kinetics were characterised by multi-phasic degradation patterns and the results indicated degradation rate is affected by light intensity and polymer thickness. Mass balance analysis indicates that losses of volatile materials to the air compartment may also be occurring.
Article
The effects of ZnO nanoparticles (NPs) interacting with single-celled green algae, Chlorella sp., have been found to be bilateral. Specifically, our electron microscopy, plant cell, and fluorescence assays showed that the adsorption and aggregation of ZnO NPs compromised algal cell morphology, viability, and membrane integrity, resulting from zinc ion dissolution as well as possible mechanical cell damage induced by the NPs. Conversely, algal cells displayed a remarkable capability of self-protection by minimizing their surface area through aggregation mediated by the oppositely charged metal ions and suppressing zinc ion release from the NPs through exudation, as evidenced by inductively coupled plasma mass spectrometry, zeta potential, and attenuated total reflectance-Fourier transform infrared spectroscopy. This study illustrates the adaptive nature and complexity in potential ecological response to discharged nanomaterials.