Intergenerational and biological effects of roxithromycin and polystyrene microplastics to Daphnia magna (2023)

Aquatic Toxicology

Volume 248,

July 2022

, 106192

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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.

Section snippets

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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