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The influence of microplastics (MPs) on transgenerational effects of pharmaceuticals are drawing growing attention, however, whether aged process will alter the carrier effects of MPs were unknown. In this study, the intergenerational toxicity of single and combined exposure of polystyrene microplastics (PS-MPs) and roxithromycin (ROX) were investigated at the environmentally related concentrations, using Daphina magna as test organism. In the presence of UV-aged PS-MPs, the survival of D. magna for maternal generation (F0) at ROX concentration of 0.1 and 10 µg/L were increased by 20% and 40%, respectively. Meanwhile, the inhibition effects of ROX on the number of offspring and intrinsic rate of natural increase were obviously moderated. All these reproductive toxicity of ROX and PS-MPs in the first offspring (F1) were further aggravated both for the single and combined exposure. And the adverse effects disappeared much easier for the single exposure compared to the co-exposure through subsequent recovery. The combined exposure resulted in the change of inhibition of ROX on the swimming velocity and acceleration of D. magna into induction, while the feeding behavior kept inhibited. The AChE activity was distinctly increased by 1.61-3.25 times for the single and combined treatments, and the induction level of UV-aged MPs was higher than that of original MPs. Oxidative stress of the single exposure of ROX and original PS-MPs was observed with obvious induction of T-AOC and SOD activity, while the significant increase of MDA content was observed for the co-exposure. Among all indicators, the biochemical biomarkers and time of first brood were attributed to a class among all indicators, indicating that the time of first brood might be the most sensitive reproductive toxicity index. These results illustrated that both maternal impacts and offspring quality need to be considered for assessment of interaction of emerging contaminants.
Over the last few decades, the plastic pollution has constituted a vital environmental and human health issue worldwide (Auta et al., 2017; Thompson et al., 2004). Plastic fragments gradually transformed to microplastics (MPs; 0.1 µm to 5 mm) and even nanoplastics (NPs, < 0.1 µm) under ultraviolet radiation, natural weathering, and biodegradation. The MPs/NPs have been referred as emerging pollutants and widely detected in aquatic ecosystem (Alimba and Faggio, 2019; Zhang et al., 2016). Meanwhile, the charge, roughness, porosity, polarity and hydrophobicity of particle surface were inevitably increased during the degradation and fragmentation process (Bhagat et al., 2021; Li et al., 2020). As a result, such features enable MPs to be perfect vectors for attracting more pollutants such as persistent organic pollutants, emerging contaminants and heavy metals (Elizalde-Velázquez and Gómez-Oliván, 2021; Tourinho et al., 2019; Yang et al., 2019). Increasing filed evidences emphasized the coexistence of micropollutants and MPs within aquatic food webs, stimulating a focus shift from ubiquitous occurrence to combined toxicity (Fraser et al., 2020; Fred-Ahmadu et al., 2020). Therefore, it is necessary to explore the interactive effects of environmental MPs and contaminants to reveal their adverse effects on the aquatic ecosystem.
In fact, aging process plays a crucial role in the physical and chemical characteristics of MPs in the actual aquatic environment. Compared with primary MPs, the interface behaviors of secondary MPs were relatively more active. It is indicated that surface-weathering obviously enhanced the interaction between MPs and pharmaceuticals (Fred-Ahmadu et al., 2020; Vieira et al., 2021). Pharmaceuticals tend to adsorb on weathered and aged MPs than on pristine MPs because of induced polarity on the plastic surface. Both hydrophobic and electrostatic interactions mainly govern the sorption mechanism of compounds on MPs (Atugoda et al., 2021). Meanwhile, the transformation of MPs from aqueous phase to biota phase could be affected by aging process, especially for filtered feeders (Vroom et al., 2017). Recent research has shown that the copepods Acartia longiremis and Calanus finmarchicus ingest significantly more aged-MPs beads than pristine microbeads. The aged MPs may be attributed to the formation of a biofilm, like a coating made up of natural microbes, increasing the attractiveness of the particles as food items. These evidences suggest that weathered or aged plastics are potentially more likely to be toxic than “unweathered” or pristine plastics of the same polymer type due to higher sorption of contaminants. Thus the aged MPs with high adsorption capacity could change the bioavailability of contaminants inevitably.
The antibiotics pollution has been recognized as a global environmental issue due to severe abuse and improper disposal. It is worth noting that environmental MPs were ability to associate with antibiotics,affecting the distribution, transformation and bioavailability of chemicals (Bhagat et al., 2021; Sun et al., 2021). Focus on the joint effects of MPs and antibiotics, the bioaccumulation of veterinary antibiotics was significantly enhanced with MPs sizes less than 10 µm for organisms with unselective ingestion of contaminated MPs (Han et al., 2021; Zhang et al., 2019; Zhou et al., 2020). Meanwhile, synergistic or additive effects at various levels of biological responses, including metabolic disorders, oxidative damage and growth inhibition (González-Pleiter et al., 2021; Vieira et al., 2021; Huang et al.,2020), indicated that the complex interactions in the interactive effects between MPs and antibiotics on aquatic organisms. However, a large majority of studies have only evaluated the interactive effects of MPs and antibiotics based on a short-term or single life stage. In fact, given their continuous discharge into the environment, aquatic organisms are exposed to the combined pollution throughout their entire lifetimes. Whether the intergenerational toxicity exists interactive effects under the continuous co-exposure, however, remains unclear.
Daphnia magna, representative species of freshwater zooplankton, have been preferentially selected to study the intergenerational dynamics of environmental contaminants (Jeong et al., 2016; Minguez et al., 2015a). Reproductive, behavioural and physiological parameters of D. magna are sensitive biomarkers of toxic effects of environmental stresses (Tkaczyk et al., 2021). However, the chronic tests in the OECD 211 guideline last over only one generation (OECD, 2012). The “maternal effects” (i.e., all the information about environmental disturbances transmitted from mothers to their offspring) and the health status of the offspring are not taken into account (LaMontagne and McCauley, 2001). Among them, intergenerational effects are defined as any stimulus to the parents (F0) that has measurable outcomes on the next generation (F1) (Heard and Martienssen, 2014 and Perez and Lehner, 2019). Transgenerational effects typically refer to impacts on the F2 or F3 generation due to a stimulus during the F0 generation (parents). To date, the life-history endpoints, such as survival, reproduction and growth of D. magna were negatively affected under multigenerational exposure of MPs (Luo et al., 2019; Schür et al., 2020). Intergenerational neurotoxicity, alternations of energy consumptions and transcriptional responses of D. magna caused by tetracycline were observed at the physiological and whole organism level (Kim et al., 2017; Young et al., 2014). The adverse effects can decrease the fitness of offspring, making them less adaptable to changing environments. Thus, more knowledge on intergenerational effects and recovery of aged-MPs and antibiotics co-exposure is needed to understand the interactive effects across the life history.
In the present study, the intergenerational interaction effects of aged polystyrene microplastics (PS-MPs) and roxithromycin (ROX) as well as the post-exposure recovery were investigated in D. magna populations. To examine the role of individual behavior and oxidative stress in intergenerational effects, ingestion and swimming behaviors, activities of acetylcholinesterase (AChE) and superoxide dismutase (SOD), total antioxidant capacity (T-AOC) and the content of malondialdehyde (MDA) were assessed at the end of exposure in F0. In addition, the potential risk assessment of aged PS-MPs and ROX at environmentally relevant concentrations have been also highlighted.
Chemicals and reagents
Roxithromycin (ROX, CAS: 80214-83-1, purity > 98%) was purchased from J&K Scientific Ltd (Shanghai, China). Green fluorescent PS-MPs with particle size of 5 µm (Excitation wavelength:488 nm, emission wavelength:518 nm) was purchased from Da'e Scientific Co., Ltd (Tianjin, China). The stock concentration is 10 mg/ml prepared in deionized water. The fluorescent labeled microspheres were prepared by swelling method according to the manufacturer's requirements, and the fluorescent agents were
Results and discussion
In the bioassays, the maximum changes in temperature, pH and conductivity were 0.5°C, 0.2 pH unit and 15 µS/cm in each beaker, while dissolved oxygen concentration and conductivity during the experiment were higher than 8.8 mg/L and 580 µS/cm, respectively. The mortality was below 20% in any control treatment (Fig. 2), which was fulfilled the requirements for general abiotic conditions and the criteria of OECD guidelines (OECD, 2012) for chronic bioassays with D. magna. In all biometric
Taken together, this study shows that the important effects of UV-aged PS-MPs on the intergenerational effects of ROX from the biochemical level to population level. Compared with F0, significant decrease of the number of offspring and rm as well as increase of time to birth breeding of D. magna were observed for the exposure alone of ROX at 0.1 and 10 µg/L in F1. Meanwhile, the presence of PS-MPs remarkably alleviated these adverse effects both at exposure treatment of F0 and F1. And F1 female
CRediT authorship contribution statement
Jiaqiang Liu: Methodology, Validation, Investigation, Writing – review & editing. Haohan Yang: Methodology, Validation, Conceptualization, Formal analysis, Investigation, Writing – original draft, Writing – review & editing. Qingjun Meng: Supervision, Investigation. Qiyan Feng: . Zhenhua Yan: Writing – review & editing, Project administration. Jianchao Liu: Writing – review & editing, Project administration. Zhigang Liu: Project administration. Zhengxie Zhou: Project administration.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
This study was supported by the Fundamental Research Funds for the Central Universities (Grant No. 2021QN1034). The Science and Technology Plan Projects of Xuzhou City (Grant No. KC19218).
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Citation Excerpt :
D. magna was found to be sensitive to a large number of chemicals (Hanazato, 1998). The commonly sensitive biomarkers include mortality, body length, swimming behavior, number of cumulative molts, total protein, oxidative stress, antioxidant enzyme activities, neurotoxicity, chronic reproduction (e.g. days to first brood, number of broods and neonates) (Felten et al., 2020; Liu et al., 2022a) (Fig. 4) (Table S2). Daphnia has been shown to be susceptible to PTEs (Murano et al., 2007).
This review considers the interaction of microplastics (MPs)/nanoplastics (NPs) and co-existing contaminants, including organic contaminants, potentially toxic elements (PTEs), and metal/metal-oxide nanoparticles. Stronger adsorption between plastic particles and co-existing contaminants can either facilitate or prevent more contaminants to enter plankton. The characteristics of MPs/NPs, such as polymer type, size, functional groups, and weathering, affect combined effects. Mixture toxicity is affected by those factors simultaneously and also affected by the type of co-existing contaminants, their concentrations, exposure time, dissolved organic matter, and surfactant. For co-exposure involving organics and metal nanoparticles, marine Skeletonema costatum generally had antagonistic effects, while marine Chlorella pyrenoidosa, Platymonas subcordiformis, and Tetraselmis chuii, showed synergistic effects. For co-exposure involving organics and PTEs, both Chlorella sp. and Microcystis aeruginosa generally demonstrated antagonistic effects. Freshwater Chlorella reinhardtii and Scenedesmus obliquus had synergistic effects for co-exposure involving metal/metal oxide nanoparticles. Zooplankton shows more unpredicted sensitivity towards the complex system. Different co-existing contaminants have different metabolism pathways. Organic contaminants could be biodegraded, which may enhance or alleviate mixture toxicity. PTEs could be adsorbed and desorbed under changing environments, and further affect the combined effects. The presence of metal/metal-oxide nanoparticles is more complicated, since some may release ion metals, increasing contaminant composition.
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Chemosphere, Volume 290, 2022, Article 133362
The widespread application of zinc oxide nanoparticles (ZnO NPs) has raised concerns over the adverse effects on aquatic species. In this study, transcriptomic analysis was applied to evaluate the chronic toxicity of ZnO NPs on the freshwater invertebrate Daphnia magna and the intergenerational effects were then further investigated. Parent daphnia (F0) were exposed to ZnO NPs at 3, 60, and 300μgL−1 for 21 days. ZnO NPs significantly inhibited the reproduction (first pregnancy and spawning time, total number of offspring) and growth (molting frequency and body length) of F0. Here, differentially expressed genes (DEGs) involved in lysosomal and phagosome, energy metabolism and endocrine disruption pathways were significantly downregulated. Furthermore, disruption on the transport and catabolic processes probably resulted in the particle accumulation. The inhibited pathways related to energy metabolism may partially account for the body length, molting and reproductive restriction. The suppression of growth and reproduction may attribute to the down-regulation of insulin secretion and ovarian steroidogenesis pathways, respectively. Partial recovery of growth and reproductive inhibition in F1 – F3 descended from the F0 generation exposure did not support constant transgenerational effects. This study unravels the molecular mechanisms and transgenerational consequences of the toxicity of nanoparticles on Daphnia.
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Journal of Hazardous Materials, Volume 427, 2022, Article 127913
Microplastics are an emerging and increasingly serious pollutant in freshwater environment, which have become a threat to freshwater organisms. However, whether microplastics interfere with the responses of organisms to their predators is still unclear. In this study, we investigated the effects of microplastics with tiny different particle size (diameter: 0.7 and 1µm) on the anti-predation (Rhodeus ocellatus as the predator) defense responses of different body-sized cladocerans, Daphnia pulex and Moina macrocopa. Results showed that microplastics had a size-based inhibitory effect on the induced defense of both D. pulex and M. macrocopa. Specifically, 0.7µm microplastics had stronger effects on reduced survival time, delayed maturation time, and decreased offspring numbers. In addition, the effects of microplastics also varied with different body-sized cladocerans, i.e. medium-sized cladoceran (D. pulex) were more sensitive than the small-sized one (M. macrocopa) regarding the maturation time. This study illustrated for the first time that the effect of microplastics on induced defense was related to cladoceran species and microplastics size, and further revealed the extensive negative effects of microplastics from the perspective of interspecific relationship.
Bioavailability of citalopram to Daphnia magna in the presence of suspended sediments with various properties
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The influence of suspended sediment (SPS) properties on the biological effects of antidepressant citalopram (CIT) was investigated in our study. For CIT exposure alone, the feeding behavior, energy available, glutathione-S-transferase (GST) activity of D. magna were vitally induced at 10μg/L. In the presence of SPS, significant dose-dependent reduction in the ingestion and filtration rates were observed with the increase of SPS concentration, while SPS organic content (foc) of 1% exhibited the most serious aggravation. The protein was the main contributor to detoxification and cellular protection under the stress of CIT and SPS. Obvious disturbance effects on the malonaldehyde content, catalase and GST activities were observed for SPS of 0.1g/L, 60–90μm and foc of 2%. Overall, the important role of SPS properties on the biological effects of CIT should be taken into consideration for the accurate risk assessment of pollutants.
Mediated food and hydrodynamics on the ingestion of microplastics by Daphnia magna
Environmental Pollution, Volume 251, 2019, pp. 434-441
There is consensus on the need to study the potential impact microplastics (MP) have on freshwater planktonic organisms. It is not yet fully understood how MP enter the aquatic food web or the effect they have on all the trophic levels. As a result of the potential for MP to accumulate throughout food webs, there is increasing interest in evaluating their fate in a variety of environmental conditions. This study investigated the variability in the ingestion of MP to food ratios and the exposed time of MP to Daphnia magna in non-sheared and sheared conditions. The sheared environment provided Daphnia magna with the conditions for optimal filtering capacity. Regardless of the ratios of MP concentration to food concentration (MP:Food), the filtration capacity of the Daphnia magna was enhanced in the sheared experiments. In both the sheared and non-sheared experiments, filtration capacity decreased when the ratios of MP to food concentration and the exposure times to MP were increased. Mortality was mainly enhanced in the non-sheared conditions at higher MP concentrations and exposure times to MP. No mortality was found in the sheared conditions for the exposure times studied. Therefore, in aquatic systems that undergo constant low sheared conditions, Daphnia magna can survive longer when exposed to MP than in calm conditions, provided food concentrations do not limit their capacity to filter.
Polystyrene microplastics ingestion induced behavioral effects to the cladoceran Daphnia magna
Chemosphere, Volume 231, 2019, pp. 423-431
Microplastic (μPs) contamination represents a dramatic environmental problem threatening both aquatic and terrestrial organisms. Although several studies have highlighted the presence of μPs in aquatic environments, the information regarding their toxicity towards organisms is still scant. Moreover, most of the ecotoxicological studies of μPs have focused on marine organisms, largely neglecting the effects on freshwater species. The present study aimed at exploring the effects caused by 21-days exposure to three concentrations (0.125, 1.25 and 12.5 μg/mL) of two differently sized polystyrene microplastics (PμPs; 1 and 10 μm) to the Cladoceran Daphnia magna. The ingestion/egestion capability of daphnids (<24 h) and adults, the changes in individual growth and behavior, in terms of changes in swimming activity, phototactic behavior and reproduction, were investigated. Both particles filled the digestive tract of daphnids and adults within 24 h of exposure at all the tested concentrations. Ingested PμPs remained in the digestive tract even after 96 h in a clean medium. For both particles, an overall increase in body size of adults was noted at the end of the exposure to the highest tested concentrations, accompanied by a significant increase in swimming activity, in terms of distance moved and swimming velocity, and by an alteration of the phototactic behavior. A significant increase in the mean number of offspring after the exposure to the highest PμPs concentrations of different size was recorded. Polystyrene μPs can affect behavioral traits of D.magna leading to potentially harmful consequences on population dynamics of this zooplanktonic species.
Effects of nanoplastics at predicted environmental concentration on Daphnia pulex after exposure through multiple generations
Environmental Pollution, Volume 256, 2020, Article 113506
The biological effects of nanoplastics are a growing concern. However, most studies have focused on exposure to high concentrations or short-term exposure. The potential effects of exposure to low environmental nanoplastic concentrations over the long-term and across multiple generations remain unclear. In the present study, Daphnia pulex was exposed over three 21-day generations to a typical environmental nanoplastic concentration (1 μg/L) and the effects were investigated at physiological (growth and reproduction), gene transcription and enzyme activity levels. Chronic exposure did not affect the survival or body length of D.pulex, whereas the growth rate and reproduction were influenced in the F2 generation. Molecular responses indicated that environmental nanoplastic concentrations can modulate the response of antioxidant defenses, vitellogenin synthesis, development, and energy production in the F0-F1 generations, and prolongation resulted in inhibitory effects on antioxidant responses in F2 individuals. Some recovery was observed in the recovery group, but reproduction and stress defenses were significantly induced. Taken together, these results suggest that D.pulex recovery from chronic exposure to nanoplastic may take several generations, and that nanoplastics have potent long-term toxic effects on D.pulex. The findings highlight the importance of multigenerational and chronic biological evaluations to assess risks of emerging pollution.
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