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Article

Combined Toxicity of Polystyrene Nanoplastics and Pyriproxyfen to Daphnia magna

by
Hua-Bing Jia
,
Yu-Hang Zhang
,
Rong-Yao Gao
,
Xiao-Jing Liu
,
Qian-Qian Shao
,
Ya-Wen Hu
,
Li-Min Fu
* and
Jian-Ping Zhang
*
Key Laboratory of Advanced Light Conversion Materials and Biophotonics, Department of Chemistry, Renmin University of China, Beijing 100872, China
*
Authors to whom correspondence should be addressed.
Sustainability 2024, 16(10), 4066; https://doi.org/10.3390/su16104066
Submission received: 26 March 2024 / Revised: 10 May 2024 / Accepted: 11 May 2024 / Published: 13 May 2024
(This article belongs to the Special Issue Emerging Contaminants in the Environment: Measurement, Transport, Impacts, Bioaccumulation, and Remediation)
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Abstract

:
In recent years, the adverse effects of nanoplastics (NPs) and pyriproxyfen on aquatic environments have attracted widespread attention. However, research on their combined exposure to aquatic organisms could be more extensive. This work evaluated the acute and chronic toxic effects of polystyrene NPs (PS-NPs) and pyriproxyfen on Daphnia magna (D. magna) under their combined exposure conditions. The addition of PS-NPs within 24 h reduced the acute toxicity of pyriproxyfen to D. magna, resulting in an increase in the 24-h EC50 values of pyriproxyfen on D. magna from 0.24 mg/L to 0.35, 0.51, and 1.26 mg/L, respectively when 1, 5, and 10 mg/L of PS-NPs were added. Compared with PS-NPs, pyriproxyfen significantly disturbed the growth and reproduction of D. magna in the chronic toxicity test at 21 days. The adverse effects caused by pyriproxyfen were alleviated when PS-NPs and pyriproxyfen were co-exposed. In addition, it was observed that the addition of pyriproxyfen resulted in less PS-NPs uptake by D. magna using a time-gated imaging technique. These findings provide new insight into the combined toxic effects of NPs and pyriproxyfen on the reproduction and growth of D. magna, and it is important to understand the effects of complex pollutants on aquatic systems. Moreover, it has provided an important scientific basis for environmental protection and sustainable development.

1. Introduction

Plastic pollution has emerged as a significant issue, garnering widespread attention. Plastics transform into microplastics (MPs) and nanoplastics (NPs) through exposure to UV radiation and mechanical wear [1,2], subsequently entering aquatic ecosystems [3,4,5]. Aquatic organisms inadvertently ingest these plastics, leading to their accumulation within their bodies [6,7,8]. This perpetual accumulation triggers adverse effects at the cellular, subcellular, and tissue levels, encompassing tissue damage [9,10], oxidative stress [11,12,13,14,15], induced lipid accumulation [16,17,18,19], metabolic disorders [20], digestive tract obstruction or injury [21], and disruption in growth and reproduction [17,22]. NPs (<1000 nm), being several orders of magnitude smaller than MPs, are more prone to absorption and concentration within aquatic organisms [23,24]. Evidence suggests that NPs pose a more significant toxicity to freshwater animals than MPs [25,26]. NPs possess a high specific surface area and unique surface properties [27], enabling them to interact with heavy metals and persistent organic pollutants, exerting complex biological effects through various pathways. For instance, NPs can adsorb organic pollutants like phenanthrene, and polychlorinated biphenyls [28,29], ZnO nanoparticles [30], and even secrete proteins [31], enhancing their toxicity towards D. magna. Additionally, NPs can alter the freely dissolved concentration of heavy organic chemicals (HOCs) and modulate their toxicity to biota, thereby influencing these pollutants’ environmental distribution and ecotoxicity of these pollutants [32,33,34]. Therefore, it is imperative to investigate the toxic effects of NPs combined with other pollutants on aquatic organisms.
Pyriproxyfen is a juvenile hormone analog insecticide with a strong ability to control flies, mosquitoes, and cockroaches. It exhibits relative environmental stability and is classified as a persistent pollutant. In aerobic water, its half-life is 23.1 days, while in anaerobic water, it can reach up to 288.9 days [35]. According to the New York State risk assessment, the estimated pyriproxyfen concentration in aquatic systems is 93 ng/L. However, this concentration may surge closer to 400 ng/L following a spraying session lasting 24 h [36]. While pyriproxyfen poses low toxicity to mammals and birds, it can potentially harm non-target organisms, such as fish and crustaceans [37,38,39]. Previous studies have revealed that pyriproxyfen disrupted the endocrine system of D. magna [40], adversely affected its mortality, fertility and growth, and even induced D. magna to produce male offspring [41,42,43].
D. magna is a filter-feeding animal, representing a significant group of aquatic organisms. It serves as food for fish and functions as a crucial link in the aquatic food chain. D. magna offers numerous practical advantages in experimental settings, including ease of cultivation under laboratory conditions, a short life cycle, and high sensitivity to environmental pollutants and other stressors [44]. The sensitive behavioral and physiological responses exhibited by D. magna are utilized as biomarkers for assessing the effects of various environmental factors and chemical substances. This property is commonly employed in fixation, lethality, and reproductive tests [45,46]. D. magna has been used to study the short- or long-term effects of pollutants such as nanoparticles [47,48], pharmaceuticals [49], metals [50], and pesticides [51]. Moreover, studies on the effects of combined pollutants on D. magna have received wide attention [52,53].
Studies on the effects of NPs and other pollutants (such as endocrine disruptors) on the growth and reproduction of D. magna have been limited [54,55]. However, the growth and reproduction of organisms are critical indicators for assessing the long-term ecological risks of pollutants. In addition, most studies use pollutant concentrations that are often much higher than ambient concentrations, which may overestimate the effects of pollutants on aquatic organisms [56,57]. As polystyrene is one of the most commonly used plastic polymers in the world [58], this study selected polystyrene nanoplastics as model nanoplastics to evaluate the acute and chronic toxicological effects of PS-NPs and pyriproxyfen at different concentrations on D. magna. The experimental protocol analyzed key growth and reproductive parameters of D. magna were conducted, including molting condition, reproductive capacity, and body length. Moreover, the absorption of NPs in D. magna was examined when the organisms were co-exposed to the pollutants. These data are imperative for elucidating the environmental hazards these pollutants pose to aquatic ecosystems, facilitating informed decisions towards environmental preservation and sustainable development strategies.

2. Materials and Methods

2.1. Polystyrene Nanoplastics

Upconversion nanoparticles of NaLuF4: 20% Yb, 2% Er were prepared using the traditional solvothermal method. NaLuF4: 20% Yb, 2% Er@NaLuF4 (UCNPs) were synthesized by coating a layer of NaLuF4 shell onto NaLuF4: 20% Yb, 2% Er upconversion nanoparticles [59,60]. The preparation of UCNPs@SiO2 colloids involved a slightly modified inverse microemulsion method. Finally, UCNPs@SiO2@PS were synthesized using a two-step dispersion polymerization technique [61]. More detailed information is shown in Supporting Information (SI) (Figure S1). PS-NPs exhibiting upconversion luminescence can be utilized to identify and locate NPs absorbed by aquatic organisms.

2.2. Test Chemicals

Macklin supplied pyriproxyfen, CAS: 95737-68-1, with a purity of 97%. The chemical’s formal name is 2-(1-Methyl-2-(4-phenoxyphenoxy)ethoxy) pyridine.
For experimental purposes, we prepared various concentrations of pyriproxyfen solutions. Pyriproxyfen was dissolved in ethanol, resulting in a final ethanol concentration of up to 2%. Prior laboratory tests had demonstrated that this ethanol concentration had no impact on the survival or reproduction of D. magna.

2.3. Organism Culture

The D. magna specimens were sourced from Tuokesi Technology Co., Ltd., Tianjin, China and cultured in Elendt M4 medium (OECD, Paris, France, 2012) in a 500 mL beaker with 500 mL of Elendt M4 medium. The test subjects were derived from healthy parthenogenesis cultures, exhibiting no signs of stress, such as the emergence of males or ephippia. The temperature was maintained at 20 ± 1 °C during the incubation, and a 16/8 h light–dark cycle was performed under a cool white fluorescent lamp (1000 lux). Chlorella sp. was fed to D. magna three times a week. Elendt M4 medium was changed weekly. According to OECD recommendation (OECD, 2012), third-generation individuals (<24 h) were used for the test.

2.4. Design of Test

2.4.1. Acute Toxicity Test

In order to study the acute toxicity of pyriproxyfen to D. magna, both alone and in combination with PS-NPs, an immobilization test was carried out on D. magna as recommended by the OECD recommendation (OECD, 2004). These tests aimed to establish the concentration of pyriproxyfen required to immobilize 50% of D. magna individuals after a 24-h exposure period. Neonates born within the last 24 h were selected and were not fed throughout the test. A small beaker of 100 mL was filled with 80 mL of solution, and then ten neonates were placed inside. In order to prevent evaporation of the solution and other potential influences, the beaker was covered with a layer of plastic wrap. Neonates were considered immobilized if they were unable to swim after 15 s of light agitation. The concentration of pyriproxyfen was selected by reference to SI (Table S1). Each test was repeated three times.

2.4.2. Chronic Toxicity Test

The 21-day exposure was based on the OECD recommendation (OECD, 2004). The concentrations of PS-NPs used in this test were 0, 100, 250, 500, 1000 µg/L, and the concentrations of pyriproxyfen were 0, 100, 200 mg/L. A semi-static test setup was used, in which a neonate was placed in a 25 mL glass beaker with 15 mL of Elendt M4 medium, and six replicates were performed for each group. The medium was changed every two days, and the density of chlorella sp. used for feeding was 2 × 106 cells/mL.
The offspring produced by each D. magna and the number of molts per D. magna were counted and removed daily. Survival and reproduction of D. magna were monitored and recorded every day. The number of molts, time to first brood, number of broods, the total number of offspring, and body length were the criteria used to evaluate the fecundity and viability. The length of each adult female, from the apex of the helmet to the base of the tail spine, was measured with stereo-microscope and imaging software (Figure S2).

2.5. Nanoplastics (NPs) Uptake

Combining of polystyrene-encapsulated UCNPs with our self-developed time-gated imaging (TGI) technique allowed us to observe the distribution of UCNPs in D. magna using noninvasive methods. This approach effectively eliminated the interference from the excitation of stray light and bio-autofluorescence, enabling in situ imaging of PS-NPs without compromising the original morphology of the biological samples [62,63]. To assess the impact of various concentrations of pyriproxyfen on the uptake of PS-NPs by D. magna neonates (<24 h), we selected concentrations of 0, 500, 1000, and 2000 ng/L for pyriproxyfen and 1 and 5 mg/L for PS-NPs. The PS-NPs content in the neonates’ bodies was measured after a 12-h exposure period. The D. magna neonates were not fed during the entire experiment. Each concentration was tested ten times to ensure reproducibility.

2.6. Statistical Analysis

The EC50 was fitted using GraphPad prism, the body length of D. magna was statistically analyzed using Image J, and IBM SPSS Statistics was used for statistical analysis. The experimental data were subjected to homogeneity of variance tests. ANOVA tests versus Dunnett’s Multiple Comparison post hoc test were used to determine significant differences between the control group and the test group. All data were represented as mean ± standard deviation. The significant level was set at p < 0.05.

3. Results

3.1. Acute Toxicity Test of Pyriproxyfen

This study evaluated the acute toxicity of pyriproxyfen on D. magna. In a 24-h acute toxicity test, pyriproxyfen caused immobilization of D. magna, resulting in a measured 24-h EC50 value of 0.24 mg/L, as shown in Figure 1A. This EC50 value aligns with the 0.26–0.42 mg/L range reported in previous studies [64]. When PS-NPs were added to the solution at concentrations of 1, 5, and 10 mg/L, the EC50 values increased to 0.35 mg/L (Figure 1B), 0.51 mg/L (Figure 1C), and 1.26 mg/L (Figure 1D), respectively. A distinct trend emerged, indicating a positive correlation between PS-NPs concentration and the observed response. Based on these findings, we hypothesize that the presence of PS-NPs reduced the acute toxicity of pyriproxyfen towards D. magna.

3.2. Effects of Pyriproxyfen and Polystyrene Nanoplastics (PS-NPs) on the Growth and Reproduction of D. magna

3.2.1. Molting Condition

During the 21-day exposure period to the contaminant, no deaths of D. magna were recorded. Furthermore, there was no significant difference in the number of molts when D. magna were exposed solely to PS-NPs (Figure 2). The addition of 100 ng/L pyriproxyfen did not produce a notable effect. However, a significant increase in molts was observed when the concentrations of pyriproxyfen and PS-NPs were raised to 200 ng/L and 1 mg/L, respectively. Molting is a crucial biological process for crustaceans, vital for growth, development, and reproduction [65]. In this study, both PS-NPs and pyriproxyfen altered the number of molts in D. magna, albeit non-significantly. Nevertheless, these findings suggest that the impact of PS-NPs and pyriproxyfen as pollutants on the developmental processes of D. magna cannot be overlooked, as these effects may manifest over the long term.

3.2.2. Reproductive Condition

During the 21-day test, the control group exhibited a time to first brood per female of 8.2 days. Exposure to various concentrations of PS-NPs did not significantly affect this time frame (Figure 3A). However, a notable delay in the time to first brood was observed when D. magna were exposed to pyriproxyfen. Specifically, the time was delayed by 1.3 and 2.6 days with the addition of 100 ng/L and 200 ng/L of pyriproxyfen, respectively. Interestingly, when compared to exposure to pyriproxyfen alone, the time to first brood was significantly shorter when D. magna were co-exposed to both PS-NPs and pyriproxyfen.
Furthermore, throughout the entire 21-day test period, the times of broods per female were recorded. Upon exposure to PS-NPs, it was discovered that the times of broods per female increased once. Conversely, pyriproxyfen did not have a notable impact on the times of broods. Nevertheless, a noticeable upward trend was observed in the number of broods per female when D. magna were simultaneously exposed to both PS-NPs and pyriproxyfen (Figure 3B).
When exposed to PS-NPs, D. magna did not show a significant change in the number of offspring per brood. In contrast, pyriproxyfen significantly reduced the number of offspring per brood. The number of offspring per brood decreased by 30% and 70%, respectively, when 100 ng/L and 200 ng/L of pyriproxyfen were added (Figure 3C). Interestingly, when D. magna were co-exposed to both PS-NPs and pyriproxyfen, PS-NPs seemed to mitigate the negative impact of pyriproxyfen on offspring numbers. Compared to D. magna exposed to the same concentrations of pyriproxyfen alone, the offspring count increased by up to 19% and 78% when co-exposed (Figure 3C).
During the 21-day test, the control group produced 160 offspring. When exposed to PS-NPs alone, the total number of offspring per female exhibited an upward trend with increasing concentrations, resulting in a 4–21% increase. Conversely, exposure to pyriproxyfen alone significantly decreased the total number of offspring per female, with higher concentrations resulting in steeper declines (Figure 3D). Specifically, the number of offspring decreased by 30% and 73% when 100 ng/L and 200 ng/L pyriproxyfen were added, respectively, compared to the control group. Notably, there was an interaction between PS-NPs and pyriproxyfen. When D. magna were co-exposed to both, the decrease in offspring numbers was alleviated, and the total number of offspring per female significantly increased with higher concentrations of PS-NPs. Compared to D. magna exposed to the same concentrations of pyriproxyfen alone, the number of offspring increased by up to 31% and 66% when co-exposed.

3.2.3. Growth Situation

PS-NPs enhanced the body length of D. magna as the concentrations of PS-NPs increased. At the highest concentration, the body length of D. magna increased noticeably by 0.16 mm (Figure 4). However, the addition of pyriproxyfen had a significant inhibitory effect on the body length of D. magna, with the degree of inhibition directly correlating with the concentration added. Specifically, compared to the control group, the body length decreased by 0.33 mm and 1.03 mm when 100 ng/L and 200 ng/L of pyriproxyfen were added, respectively. Furthermore, pyriproxyfen induced morphological changes in D. magna, including volume reduction and caudal spine hypoplasia (Figure S3). In the co-exposure group, we interestingly found that PS-NPs mitigated the inhibitory effect of pyriproxyfen on the body length of D. magna.

3.3. The Effect of Pyriproxyfen on Polystyrene Nanoplastics (PS-NPs) Uptake in D. magna

PS-NPs primarily concentrate in the gut of D. magna (Figure 5A,B), and the addition of pyriproxyfen did not alter the distribution. However, the presence of pyriproxyfen led to a concentration-dependent reduction in the amount of PS-NPs within D. magna. As the concentration of pyriproxyfen increased, there was a significant decrease in the PS-NPs content, especially notable in the 5 mg/L PS-NPs group (Figure 5C). At the highest concentration of pyriproxyfen, the uptake of PS-NPs was reduced by half compared to conditions without pyriproxyfen.

4. Discussion

In this work, when exposed alone, PS-NPs did not exhibit significant long-term toxicity. On the contrary, PS-NPs promoted the reproduction and growth of D. magna by increasing the times of broods, the number of offspring, and body length. This is mainly because the toxicity of NPs is closely related to their surface charge properties. Numerous studies have demonstrated that positively charged NPs are more harmful to aquatic organisms than negatively charged NPs [6]. For instance, in the acute experiment, positively charged aminated polystyrene nanoparticles (PS-NH2) exhibited the highest toxicity among the PS-NPs tested on D. magna [66]. Torre et al. also observed that after 48 h of exposure, negatively charged particles accumulated in the digestive tract of sea urchin embryos. In contrast, positively charged NPs were more widely dispersed in the gut [67]. In longer-term experiments, NPs-NH2 displayed more significant reproductive toxicity to daphnia, zebrafish, oysters, and other aquatic organisms than NPs-COOH [68,69,70]. This study used negatively charged PS-NPs with carboxyl groups on the surface. This explains why we did not observe a significant toxic effect of NPs. The weak facilitating effect of PS-NPs on D. magna may be consistent with the phenomenon of “Hormesis”, where the low concentration and hypotoxicity of environmental pollutants can promote biological responses [71,72]. Previous studies have reported that D. magna exposed to PS-NPs adjusted their energy supply by activating detoxification and antioxidant defense systems and avoided oxidative damage. At the same time, as a stress response, the feeding activities of individual daphnia are enhanced, and the total calorie intake is significantly increased, which is conducive to secondary production processes such as the growth and reproduction of D. magna [73]. Liu et al. have also found that environmental concentrations of NPs can promote the production of antioxidants, stress defense, and AMP-activated (AMPK) protein kinase in parent animals and F1 generation of D. magna, and has a specific stimulatory effect on growth and reproduction [74].
In this work, it was confirmed that pyriproxyfen, as a juvenile hormone analogue (JHA), caused adverse effects on D. magna at environmentally relevant concentrations. These effects include delayed reproduction, reduced offspring numbers, impaired physical development, and shortened body length. Given these findings, monitoring the release and transport of pyriproxyfen in aquatic environments and its potential impacts on aquatic organisms is crucial. Previous studies showed that pyriproxyfen slowed down the maturation process of D. magna, and neonates might experience developmental delays following acute exposure, and prolonged exposure can lead to irreversible damage [41]. According to research, using JHA can prevent metamorphosis and prolong the duration of the immature stage in most insects [75]. When JHA was applied to insects during their early metamorphosis, it interacted with receptor proteins, leading to abnormal development and physiological changes. Similarly, higher doses of JHA can lead to more severe defects in the central nervous system and potentially cause fatality in adult mice [76]. This can explain the acute and chronic toxicity of pyriproxyfen to D. magna at different doses. This research is consistent with previous studies, including those that 6.01 μg/L of pyriproxyfen can affect the development of D. magna, reduce reproductive rates, inhibit molting, and increase the proportion of male offspring [77]. Additionally, some studies have shown that pyriproxyfen not only affected the reproduction and growth of adult D. magna, but also significantly impacted their offspring [64].
Combined exposure to pyriproxyfen and PS-NPs significantly increased the EC50 value of pyriproxyfen against D. magna. Additionally, the 21-day chronic toxicity test demonstrated that the adverse effects of pyriproxyfen on the reproduction and growth of D. magna were alleviated by the addition of PS-NPs. This recovery effect was much stronger than the stimulatory effect of PS-NPs alone. For example, while PS-NPs alone caused a slight increase in the body length of D. magna (0.97% to 3.6%), pyriproxyfen alone significantly reduced (8.3% to 25%). Compared to exposure alone to different concentrations of pyriproxyfen, the addition of PS-NPs increased in the body length of D. magna, ranging from 1.9% to 8.2% and 4.9% to 12%, respectively. These observations suggest that the interactions between PS-NPs and pyriproxyfen are complex and not simply a superposition of their toxic effects (Figure 4). Because NPs show strong adsorption and enrichment ability to hydrophobic organic pollutants (HOCs), they can be used as carriers to change the environmental behavior of HOCs. There are many interactions related to the adsorption of HOCs on NPs, including van der Waals interaction, π–π interaction, hydrogen bond, etc. [78,79]. Meanwhile, pyriproxyfen tends to adhere to suspended solids or organic matter in the water body due to the low water solubility and high oil–water distribution coefficient [80]. Therefore, when NPs and pyriproxyfen co-exist, it is very likely that NPs adsorbed pyriproxyfen.
One explanation is that NPs tend to adsorb pyriproxyfen in aqueous solutions and then sedimentation by agglomerating, making D. magna unable to ingest this polymer of NPs and pyriproxyfen. To prove this hypothesis, a deposition test of PS-NPs was conducted after the addition of pyriproxyfen. It was found that about 36% of PS-NPs would be deposited after the addition of 100 μg/L pyriproxyfen, while no significant deposition was observed at lower concentrations (Figure S4). Although the sedimentation caused by lower concentrations of pyriproxyfen is not evident within 24 h, the contribution of this sedimentation in the long term still cannot be ignored.
Another explanation is that the toxicity of the pyriproxyfen adsorbed by NPs is likely to be significantly reduced due to its inability to contact and bind to its target site, and only the free pyriproxyfen plays a toxic role. Yang et al. discovered that MPS can decrease the effective concentration of the antibiotic ciprofloxacin (CIP) via adsorption. Furthermore, adsorption may alter the binding site of CIPs, reducing their affinity for DNA, thereby mitigating their toxicity and resulting in antagonism [81]. Along with this, Lin et al. discovered that low concentrations of NPs mitigate the toxicity of polychlorinated biphenyls (PCBs) to D. magna because the binding of NPs and the PCB reduced the free concentration of the PCB, and the PCB bound to NPs became non-toxic [82]. The acute toxicity test conducted in this study revealed that the EC50 of pyriproxyfen was 0.24 mg/L. However, upon the addition of PS-NPs concentrations of 1, 5, and 10 mg/L, the EC50 values of pyriproxyfen towards D. magna after 24 h shifted to 0.35, 0.51, and 1.26 mg/L, respectively (Figure 1). It is observable that the EC50 value increases almost linearly with the escalation of PS-NPs concentration, indicating that the toxicity of pyriproxyfen decreases as the concentration of PS-NPs increases. It can be understood that PS-NPs reduced the concentration of pyriproxyfen in the aqueous solution through adsorption, thereby mitigating its toxicity.

5. Conclusions

In this study, we observed that even at the environmentally relevant concentrations, pyriproxyfen had significant adverse effects on D. magna. This finding suggests that pyriproxyfen impacts the reproduction and growth of D. magna as an insect growth regulator and exhibits unknown short-term toxic effects. However, the presence of PS-NPs appeared to mitigate the acute toxicity of pyriproxyfen towards D. magna, alleviating its adverse impact on the reproduction and growth of D. magna. This mitigating effect may be attributed to the adsorption of pyriproxyfen by PS-NPs. Furthermore, our findings revealed that the intake of PS-NPs was inhibited by pyriproxyfen, indicating a reduction in filter-feeding efficiency. While the addition of PS-NPs in our tests reduced the toxic effect of pyriproxyfen, the long-term consequences remain unclear. Therefore, further studies are urgently needed to investigate the potential multi-generational toxic impacts of PS-NPs and pyriproxyfen on aquatic organisms, as well as the potential ecological consequences resulting from their combined exposure.
Given these concerns, it is imperative to reassess these two pollutants’ use and disposal methods to minimize their negative environmental impact and promote a more environmentally friendly and sustainable approach, thereby facilitating informed decisions towards environmental preservation and sustainable development strategies.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/su16104066/s1. Figure S1: (A) TEM image of NaLuF4: 20% Yb, 2% Er@NaLuF4@SiO2; (B) TEM images of NaLuF4: 20% Yb, 2% Er@NaLuF4@SiO2@PS; (C) diameter distribution of PS-NPs based on the result of TEM images; (D) luminescence spectrum of PS-NPs at the excitation wavelength of 980 nm (2 W/cm2). Figure S2: Measurement of body length of D. magna. Figure S3: Digital camera images of D. magna after 21 days of chronic experiment. (A) 0 ng/L pyriproxyfen; (B) 100 ng/L pyriproxyfen; (C) 200 ng/L pyriproxyfen. Figure S4: Luminescence spectrum of 1 mg/L PS-NPs at the excitation wavelength of 980 nm (2 W/cm2). Table S1: Select the concentration of pyriproxyfen.

Author Contributions

Conceptualization, H.-B.J., L.-M.F. and J.-P.Z.; funding acquisition, L.-M.F. and J.-P.Z.; methodology, H.-B.J. and L.-M.F.; investigation, H.-B.J., Y.-H.Z., R.-Y.G. and X.-J.L.; writing—original draft, H.-B.J. and L.-M.F.; writing—review and editing, H.-B.J., L.-M.F., J.-P.Z., Y.-H.Z., R.-Y.G., X.-J.L., Q.-Q.S. and Y.-W.H. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (NSFC), Grant Nos. 22076218.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data is contained within the article and Supplementary Materials.

Acknowledgments

The authors would like to acknowledge the National Natural Science Foundation of China (NSFC, Grant Nos. 22076218) for their support.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Acute toxicity of D. magna exposed to pyriproxyfen, the concentrations of PS-NPs were as follows: (A) control group; (B) 1 mg/L; (C) 5 mg/L; (D) 10 mg/L.
Figure 1. Acute toxicity of D. magna exposed to pyriproxyfen, the concentrations of PS-NPs were as follows: (A) control group; (B) 1 mg/L; (C) 5 mg/L; (D) 10 mg/L.
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Figure 2. The number of molts in D. magna during the 21-day chronic toxicity test. Different capital letters indicate a significant difference between different concentrations of pyriproxyfen at the same concentration of PS-NPs, and different lowercase letters indicate a significant difference between different concentrations of PS-NPs at the same concentration of pyriproxyfen, p < 0.05.
Figure 2. The number of molts in D. magna during the 21-day chronic toxicity test. Different capital letters indicate a significant difference between different concentrations of pyriproxyfen at the same concentration of PS-NPs, and different lowercase letters indicate a significant difference between different concentrations of PS-NPs at the same concentration of pyriproxyfen, p < 0.05.
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Figure 3. During a 21-day chronic toxicity test, the following individual parameters were measured: (A) time to first broods; (B) number of broods per female; (C) mean number of offspring per brood; (D) total offspring per female. The results were expressed as an average, n = 6. Different capital letters indicate a significant difference between different concentrations of pyriproxyfen at the same concentration of PS-NPs, and different lowercase letters indicate a significant difference between different concentrations of PS-NPs at the same concentration of pyriproxyfen, p < 0.05.
Figure 3. During a 21-day chronic toxicity test, the following individual parameters were measured: (A) time to first broods; (B) number of broods per female; (C) mean number of offspring per brood; (D) total offspring per female. The results were expressed as an average, n = 6. Different capital letters indicate a significant difference between different concentrations of pyriproxyfen at the same concentration of PS-NPs, and different lowercase letters indicate a significant difference between different concentrations of PS-NPs at the same concentration of pyriproxyfen, p < 0.05.
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Figure 4. The body length of D. magna after the test, n = 6. Different capital letters indicate a significant difference between different concentrations of pyriproxyfen at the same concentration of PS-NPs, and different lowercase letters indicate a significant difference between different concentrations of PS-NPs at the same concentration of pyriproxyfen, p < 0.05.
Figure 4. The body length of D. magna after the test, n = 6. Different capital letters indicate a significant difference between different concentrations of pyriproxyfen at the same concentration of PS-NPs, and different lowercase letters indicate a significant difference between different concentrations of PS-NPs at the same concentration of pyriproxyfen, p < 0.05.
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Figure 5. Bright-field and dark-field images of PS-NPs uptake by D. magna at 12 h after the addition of pyriproxyfen. (A) 1 mg/L PS-NPs; (B) 5 mg/L PS-NPs; (C) NPs loaded in D. magna, n = 10. * p < 0.05; ** p < 0.01.
Figure 5. Bright-field and dark-field images of PS-NPs uptake by D. magna at 12 h after the addition of pyriproxyfen. (A) 1 mg/L PS-NPs; (B) 5 mg/L PS-NPs; (C) NPs loaded in D. magna, n = 10. * p < 0.05; ** p < 0.01.
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Jia, H.-B.; Zhang, Y.-H.; Gao, R.-Y.; Liu, X.-J.; Shao, Q.-Q.; Hu, Y.-W.; Fu, L.-M.; Zhang, J.-P. Combined Toxicity of Polystyrene Nanoplastics and Pyriproxyfen to Daphnia magna. Sustainability 2024, 16, 4066. https://doi.org/10.3390/su16104066

AMA Style

Jia H-B, Zhang Y-H, Gao R-Y, Liu X-J, Shao Q-Q, Hu Y-W, Fu L-M, Zhang J-P. Combined Toxicity of Polystyrene Nanoplastics and Pyriproxyfen to Daphnia magna. Sustainability. 2024; 16(10):4066. https://doi.org/10.3390/su16104066

Chicago/Turabian Style

Jia, Hua-Bing, Yu-Hang Zhang, Rong-Yao Gao, Xiao-Jing Liu, Qian-Qian Shao, Ya-Wen Hu, Li-Min Fu, and Jian-Ping Zhang. 2024. "Combined Toxicity of Polystyrene Nanoplastics and Pyriproxyfen to Daphnia magna" Sustainability 16, no. 10: 4066. https://doi.org/10.3390/su16104066

APA Style

Jia, H.-B., Zhang, Y.-H., Gao, R.-Y., Liu, X.-J., Shao, Q.-Q., Hu, Y.-W., Fu, L.-M., & Zhang, J.-P. (2024). Combined Toxicity of Polystyrene Nanoplastics and Pyriproxyfen to Daphnia magna. Sustainability, 16(10), 4066. https://doi.org/10.3390/su16104066

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