Combined effects of ZnO nanoparticles and toxic Microcystis on life-history traits of Daphnia magna

Chemosphere 233 (2019) 482e492

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Combined effects of ZnO nanoparticles and toxic Microcystis on lifehistory traits of Daphnia magna Yuanyuan Wang a, Shanshan Qin a, Yurou Li a, Guangjin Wu a, Yunfei Sun a, Lu Zhang a, Yuan Huang a, Kai Lyu a, Yafen Chen b, Zhou Yang a, * a

Jiangsu Key Laboratory for Biodiversity and Biotechnology, School of Biological Sciences, Nanjing Normal University, 1 Wenyuan Road, Nanjing, 210023, China State Key Laboratory of Lake and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, 73 East Beijing Road, Nanjing, 210008, China b

h i g h l i g h t s

g r a p h i c a l a b s t r a c t


Daphnia live in aquatic environment where Microcystis and NPs coexist.
Both toxic Microcystis and NPs delayed the development of Daphnia.
Both toxic Microcystis and NPs reduced reproductive performance of Daphnia.
There was a significant interaction between NPs and food on Daphnia's reproduction.
NPs and toxic Microcystis mutually attenuate their harmful effects on Daphnia.

a r t i c l e i n f o

a b s t r a c t

Article history: Received 2 April 2019 Received in revised form 26 May 2019 Accepted 29 May 2019 Available online 3 June 2019

Rise in cyanobacterial blooms and massive discharge of nanoparticles (NPs) in aquatic ecosystems cause zooplankton to be exposed in toxic food and NPs simultaneously, which may impact on zooplankton interactively. Therefore, the present study focused on assessing the combined effects of different ZnO NPs levels (0, 0.10, 0.15, 0.20 mg L1) and different proportions of toxic Microcystis (0%, 10%, 20%, 30%) in the food on a model zooplankton, Daphnia magna. The results showed that both toxic Microcystis and ZnO NPs significantly delayed the development of D. magna to maturation, but there was no significant interaction between the two factors on the times to maturation except the body length at maturation. Both ZnO NPs and toxic Microcystis also significantly decreased the number of neonates in the first brood, total offspring, and number of broods per female, and there was a significant interaction between ZnO NPs and food composition on the reproductive performance of D. magna. Specifically, presence of toxic Microcystis reduced the gap among the effects of different ZnO NPs concentrations on the reproductive performance of D. magna. When the ZnO NPs concentration was at 0.15 mg L1, the gap of the reproductive performance among different proportions of toxic Microcystis also tended to be narrow. Similar phenomenon also occurred in mortality. Such results suggested that low concentration of ZnO NPs and toxic Microcystis can mutually attenuate their harmful effects on D. magna, which has significantly implications in appropriately assessing the ecotoxicological effects of emerging pollutants in a complex food conditions. © 2019 Elsevier Ltd. All rights reserved.

Handling Editor: Tamara S. Galloway Keywords: Daphnia magna Food types Life history Toxic Microcystis ZnO nanoparticles

* Corresponding author. E-mail address: [email protected] (Z. Yang). https://doi.org/10.1016/j.chemosphere.2019.05.269 0045-6535/© 2019 Elsevier Ltd. All rights reserved.

Y. Wang et al. / Chemosphere 233 (2019) 482e492

1. Introduction Metal oxide nanoparticles (NPs) are among the most studied NPs widely used in various fields (e.g. industry, agriculture) due to their well-known chemico-physical properties (Barrena et al., 2009; Kahru and Dubourguier, 2010; Hu and Cao, 2019). ZnO NPs is one of the most commonly used metal oxide NPs in industrial and daily supplies (Ma et al., 2013; Jarvis et al., 2013), such as paints, cosmetics, coatings, electronics, plastics, and personal care products, with an estimated annual production of 30,000 tons (Goncalves et al., 2018), which causes the levels of ZnO NPs increasing continually in the environment. Therefore, ZnO NPs toxicity has received increasing attention as abundant different forms of ZnO NPs were released into the ecosystem (Jarvis et al., 2013). On account of their unique physical and chemical behaviors embracing large surface to volume ratio, awfully small size and high density of surface defects (Xiao et al., 2008), NPs can enter environment and spread through air, soil, and groundwater, potentially affecting the health of the organisms that live in these environments (Moore, 2006; Farre et al., 2009; Kibbey and Strevett, 2019). A large amount of studies demonstrate the toxic effects of ZnO NPs to aquatic organisms, such as prokaryotes (Premanathan et al., 2011; Yan et al., 2011; Yang et al., 2011), algae (Franklin et al., 2007; Garcia-Gomez et al., 2014; Pendashte et al., 2013), and fish (Bondarenko et al., 2013; Pirsaheb et al., 2019). Zooplankton Daphnia magna, a well-accepted model organism and standard test species in ecotoxicology (Lyu et al., 2013; Khan et al., 2019) and also playing an important role in aquatic ecosystem, are highly sensitive to ZnO NPs, showing obvious decrease in feeding, growth, reproduction, and longevity (Zhao et al., 2012; Adam et al., 2014). Eco-toxicological tests proposed that organism's sensitivity to environmental pollutants may be modified by dietary food quality and quantity (Ieromina et al., 2014; Sun et al., 2019). For example, D. magna are more susceptible to imidacloprid when fed the phosphorus-deficient diet, as observed in the lower survival and inhibited growth rate (Ieromina et al., 2014). D. magna fed vitaminenriched algae are less sensitive to a chronic copper stress than those fed vitamin-poor food (Winner et al., 2006). Furthermore, Hansen et al. (2008) found that the toxicity of a model pharmaceutical, fluoxetine, was reduced in D. magna consuming nitrogenand phosphorus-deficient food compared to those consuming relatively nutrient-rich food. Cyanobacteria are well known to be a type of low food quality for zooplankton due to toxicity (Yang et al., 2012; Lyu et al., 2016a), mechanical interference (Jarvis et al., 1987), or nutritive deficiencies (Lyu et al., 2016b). Particularly, the increased input of nutrients into lakes has led to cyanobacterial blooms occurring more frequently (O'Neil et al., 2012), which negatively affects herbivorous zooplankton, e.g. the unselective filter-feeder Daphnia (Lürling, 2003; Yang et al., 2011; Cao et al., 2014; Lyu et al., 2017). Field investigations revealed that metal oxide NPs were detected in several eutrophic lakes within a complicated environmental behavior (Xu and Jiang, 2015; Xu et al., 2016), of which the ZnO NPs were usually occurred less than 1 mg L1 (Gottschalk et al., 2009). Furthermore, as some metal oxide NPs can be applied to the remediation of eutrophic waters (da Silva et al., 2016), which may cause the persistence of NPs in waters. Consequently, the fate of ZnO NPs may interact with the major producer phytoplankton and enter the food chain, which serves as an important pathway for high trophic-level organisms absorbing and enriching nanomaterials. Hence, it is an urgent need to develop a better understanding on the interactive effects of ZnO NPs pollution and cyanobacteria on zooplankton communities to estimate aquatic grazers' fitness against changing environment.

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The aim of this study was to assess the combined effects of ZnO NPs and toxic Microcystis on D. magna, which can occur simultaneously in environment (Xu and Jiang, 2015) and may potentially result in a complex interactive effects. We formulated the hypothesis that stress caused by ZnO NPs can be disturbed by toxic effects of cyanobacteria. In order to test our hypothesis, we conducted life history experiments on D. magna by exposing the animals to the two stressors: the ZnO NPs and toxic Microcystis aeruginosa, both individually and together. 2. Materials and methods 2.1. Phytoplankton and zooplankton The freshwater crustacean Daphnia magna Straus, maintained in laboratory for over 20 years (Yang et al., 2012), was cultured in the COMBO medium (Kilham et al., 1998) which was replaced three times per week. D. magna were fed the green alga Chlorella pyrenoidosa (1.5 mg C L1) daily in 500 mL glass beakers containing 400 mL of COMBO culture medium under the conditions of 21  C and fluorescent light at 40 mmol photons m2 s1 with 14:10 h light: dark cycle. C. pyrenoidosa and toxic Microcystis aeruginosa (PCC 7806) were mass cultured separately in 1 L Erlenmeyer flasks axenically using BG-11 medium, under continuous aeration at 21  C and light intensity of 40 mmol photons m2 s1 by fluorescent light, with a light: dark period of 14 h:10 h. The cultures were manually shaken three times daily. The algae, with a single or two-cell morphs, were harvested at the exponential growth phase by centrifugation at 4500 rpm for 15 min, and then stored at 4  C as food. 2.2. Preparation and characterization of ZnO NPs test solution The ZnO NPs (diameter ¼ 50 nm, surface area >10 m2 g1) were purchased from Nanjing HaiTai Nanoparticles Ltd. The stock solution of ZnO NPs (0.10 g L1) was prepared before the exposure treatment. The particles were dispersed in Milli-Q water and then sonicated for 30 min at 40 kHz in an ice-water bath. The stock solution was then diluted into three nominal concentrations (0.10, 0.15, 0.20 mg L1) with Daphnia culture medium. The total Zn concentration in the test medium was measured using inductively coupled plasma mass spectrometry (ICP-MS, ICAP 6300, PE, USA). The shape and morphology of nanoparticles in the ZnO NPs suspension was evaluated by transmission electron microscopy (TEM, Hitachi, H-7650, Japan). Dynamic light scattering (DLS, Nicomp, Z3000) was used to characterize the zeta potential and hydrodynamic characteristics and the aggregation degree of NPs at 30 min, 24 h and 48 h, respectively. 2.3. Experimental procedure The exposure phase was consistent with the standard 21 d chronic reproduction test (OECD, 2012). D. magna neonates (less than 24 h) were obtained from the third generation of the same female. Afterwards, experimental animals were placed randomly in 50-mL beakers. Each beaker contained one experimental animal to avoid density effects (Martinez-Jeronimo et al., 2000), as well as to easily identify the performances of each individual for recording the life-history parameters. The chronic life history experiments were carried out with D. magna exposed to diverse food types combined with different ZnO NPs concentration for 21 days. The four different food types contained the same carbon biomass of 1.5 mg C L1, which is sufficient for normal growth of D. magna (Lyu et al., 2016c): (1) 100% C. pyrenoidosa (100%Ch), (2) a mixture of 90% C. pyrenoidosaþ10% toxic M. aeruginosa (90%Chþ10%Ma), (3) a

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mixture of 80% C. pyrenoidosaþ20% toxic M. aeruginosa (80% Chþ20%Ma), (4) a mixture of 70% C. pyrenoidosaþ30% toxic M. aeruginosa (70%Chþ30%Ma). We used Microcystis proportion only up to 30% in the mixed food as most of the exposed D. magna died before maturation when the proportion of M. aeruginosa exceeds 30% in food, which was proved in our preliminary experiments. Each food type was combined with four ZnO NPs nominal concentrations (0, 0.10, 0.15, 0.20 mg L-1) respectively. We used a full factorial design for each factor combination, which resulted in a total of 16 treatments (4 ZnO levels  4 diet treatments). Each treatment group contained 10 biological replicates. During the experiment, D. magna was daily transferred to clean glass beakers filled with freshly prepared nanoparticle medium and fed with fresh food mixtures indicated above. To evaluate the treatment effect, seven key life history traits were daily recorded: 1) time to maturation; 2) time to first brood; 3) body length at maturation (body length was measured from the head to the base of the spine); 4) number of neonates in the first brood per female; 5) total offspring per female; 6) number of broods per female; 7) mortality rate. During the 21-day exposure, all the experimental treatments were conducted at 21  C under photoperiod at 14:10 h light: dark cycle, and 40 mmol photon m2 s1. 2.4. Morphological observations on the algae and ZnO NPs by scanning electron microscope (SEM)

tubes at 80  C for 24 h, and then were weighed by using microbalance. Finally, the dried D. magna were digested with 5 mL of 65% HNO3 on constant temperature drying oven (at 160  C for 4e6 h). After that, digested solutions were cooled to room temperature until the acid was nearly dry, and then the digested solutions were inhaled into 25 mL vessels. The total Zn contents in the digested samples were measured by using ICP-MS and expressed as mg mg1. 2.6. Statistical analysis Data were presented as mean with the corresponding standard error (SE). Significant interactions between ZnO NPs concentrations and food types on all life history parameters (see above) were assessed via two-way ANOVA (followed by Turkey post-tests) with the except of mortality rate. The level of significance was set at a level of P < 0.05. Mortality rate (number of individual death in specific time) was obtained as the slope of accumulated number of died individuals vs. time over the 21-d experimental period or the time when all individuals died. To assess whether parameters of a single response differed between ZnO NPs concentrations under four food types separately, mortality rates among the treatments were compared with one-way ANOVA followed by Holm-Sidak method. All statistical analyses were performed with Sigma Plot 14.0. 3. Results

To further investigate how ZnO NPs affect the algae, we conducted a separate experiment. We chose the treatment of mixed food (80%Chþ20%Ma) combining with different concentrations of ZnO NPs (0, 0.10, 0.15, 0.20 mg L1) and cultured them for two days to intuitively investigate attachment of ZnO NPs on dietary algal cells. SEM were used to examine the surface structure of algae after ZnO NPs exposure. The algal cells were washed thrice with distilled water, and then were fixed in 4% glutaraldehyde. Algal cells were dehydrated from 30% to 100% in serial dilutions of ethanol and dried using a critical point dryer, and finally subjected to gold sputter coating (Hou et al., 2019). The covered-algae sample was then observed by operating at a voltage of 15 kV using the SEM (Hitachi, SU-8010, Japan). 2.5. Total Zn contents analysis Given that D. magna medium were daily renewed during the 21d ZnO NPs exposure, the real-time total Zn concentration (including the dissolved zinc ions and zinc of particles themselves) in testing solution during 24 h were measured. We set up five replicates for each exposure treatment (3 ZnO NPs levels  4 food types) with single D. magna (<24 h) in 50-mL beaker. After 24 h, the D. magna were removed and 10 mL of the remaining medium was collected uniformly. All replicates were sampled respectively. Algae were filtered off using 0.22 mm membrane filter (Millipore Corporation, USA), and the corresponding filtrates were also collected in the meantime. The collected algae and filtrates were used to measure total Zn concentrations in the algae and testing medium, respectively. In addition, the initial Zn concentrations (0 h) in the testing solution were also measured. Moreover, to determine the total Zn content accumulated in D. magna, we measured Zn content of living animals at the end of the 21-day life history experiment. Harvested D. magna samples from each treatment were transferred to Milli-Q water for 2e4 min firstly. Subsequently, they were rinsed (blow gently with a straw) twice with fresh Milli-Q water in order to roughly remove ZnO NPs from the surface. After rinsed, they were dried in pre-weighed glass

3.1. Characterization of ZnO NPs suspension As shown in Fig. 1, a photograph taken by a TEM, ZnO NPs aggregated flocculation in different shapes (including round, rectangular, and anomalous) with sizes of a few hundred nanometers in diameter. The DLS results (Fig. 1, right) showed the particle size distributed with the increase of time in the stock ZnO NPs solution, and the size of aggregated particles increased gradually. At 3, 24, and 48 h, the particle size to the peak was about 70 nm (left blue peak), 190 nm (green peak), and 220 nm (red peak), respectively, which represented the distribution of main particle sizes in the suspension. Zeta potential in the middle (3e24 h) and late stage (24e48 h) increased, specifying the system stability of this was better than that in the early stage (0e3 h). These results indicated that the NPs used in this study aggregated easily in pure water. 3.2. Measured Zn concentration in test medium, algae, and D. magna As shown in Fig. 2, the measured initial Zn concentrations in the testing solution were 0.0925, 0.1440, and 0.1920 mg L1, respectively, in the three ZnO NPs treatments. After 24-h exposure, the Zn concentrations in the three ZnO NPs treatments decreased in different degrees during 24 h (Fig. 2). Less than 10% of the initial total Zn concentrations in the testing medium was absorbed by the algae within 24 h (Fig. 3), indicating that the algae adhered a part of the Zn and it was necessary to refresh the testing solution every 24 h, aiming at adjusting ZnO NPs concentrations. Zn contents in D. magna living in the nanoparticle testing solution after 21 days showed an obvious Zn uptake of 0.029e0.0562 mg mg1 dry weight in 0.10 mg L1 treatment, 0.046e0.100 mg mg1 dry weight in 0.15 mg L1 treatment, and 0.10 mg mg1 dry weight in 0.20 mg L1 treatment, respectively (Fig. 3d). Note there was no viable D. magna in the 0.20 mg L1 ZnO NPs treatment except under the treatment of 90%Chþ10%Ma. Zn uptake in D. magna was found to be more in the case of 0.15 mg L1 ZnO NPs treatment compared to 0.10 mg L1

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Fig. 1. TEM images of ZnO NPs dispersions of 50 nm in Millio-Q water (left) and Number-WT Nicomp distribution of ZnO NPs suspension (0.10 g L1) with different time (Purple line 0 h, Blue line 3 h, Green line 24 h, Red line 48 h) (right). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

treatment, indicating uptake of ZnO NPs was dependent on concentration of accumulated ZnO particles in the test solution.

had a weakening effect on the toxicity of ZnO NPs to D. magna in a certain range mutually.

3.3. Morphological observations on algal cells

3.5. Daphnia development (time and body length at first maturation)

Algal cells were generally round and had a smooth exterior without NPs exposure (Fig. 4A). When exposed to NPs, surface of some algal cells were covered with NPs (Fig. 4B). The higher the NPs concentration was, the more cells were covered with NPs, and also the more substances were adhered on the surface of cells. Some cells were severely deformed and shrunk under high level of NPs exposure (Fig. 4C). These results were in harmony with previous findings that the NPs can form aggregates in the medium that capture and encapsulate the algae cells. 3.4. Mortality rate Mortality of D. magna occurred in all exposure treatments, except the treatments without the ZnO NPs under the food of 100% Ch (Fig. 5). When not exposed to the ZnO NPs, the mortality rate of D. magna increased with the increase of proportions of toxic Microcystis in the food. As ZnO NPs concentrations increased, mortality rate significantly increased when D. magna were fed by pure Chlorella (Fig. 5a). At the food treatment of low proportion (10%) of toxic Microcystis (Fig. 5b), one-way ANOVA showed there was no significant difference in mortality as the concentration of ZnO NPs increased, and the upward trend moderated. Interestingly, with the proportion of Microcystis increased, the mortality rate of maternal Daphnia exposed to ZnO NPs at 0.10 and 0.15 mg L1 were all significantly lower than the treatment without ZnO NPs under the mixed food of 80%Ch þ20%Ma (Fig. 5c) and 70%Ch þ30%Ma (Fig. 5d), respectively. Nevertheless, the mortality rate then amounted the maximum when the concentration of ZnO NPs was the highest (0.20 mg L1) of each food treatment, and a significant difference in mortality was detected (Holm-Sidak method). Another interesting phenomenon also happened in the treatment of food combined toxic Microcystis. When compared to pure good food treatment (100%Ch), the mortality in the treatment of (90%Ch þ10%Ma) and (80%Ch þ20%Ma) decreased under the ZnO NPs concentration of 0.10 and 0.15 mg L1, respectively. Nevertheless, the mortality rate then amounted the maximum with the highest proportion of toxic Microcystis (70%Ch þ30%Ma) of each ZnO NPs level. The results indicated that the toxicity of Microcystis

Both proportion of Microcystis in the food types and ZnO NPs concentrations significantly delayed the times of maturation and first brood, while there was no interaction between the two factors on the times (Table 1). In all four ZnO levels, the time to maturation (first batch of eggs) and the time to first brood significantly delayed with increasing proportions of toxic Microcystis (P < 0.05, Fig. 6). Moreover, the higher proportion of M. aeruginosa and higher ZnO NPs concentration had a synergistic effect on increase in terms of the times (as shown above). Regarding the body length at maturation, significant effects were observed among the four food types (P < 0.01, Fig. 6c), except no individual reproduced in the food type of 70%Chþ30%Ma under 0.20 mg L1 ZnO NPs, whereas there was no significant effect on the body length for the factor of ZnO NPs concentrations. When the ZnO NPs concentration was 0 mg L1, the body length decreased linearly with the increase of the proportion of toxic Microcystis, however, with the increase of the ZnO NPs concentration, the decline trend became relaxed, indicating that ZnO NPs may buffer the detrimental effects of toxic Microcystis on D. magna. Two-way ANOVA also suggested there was a significant interaction between food types and ZnO NPs concentrations on the body length at maturation (Table 1). 3.6. Daphnia reproduction performance Two-way ANOVA showed both the food types and ZnO NPs concentrations had significant effects on the three reproduction parameters (neonates of first brood per female, total offspring per female, number of broods per female), respectively, and there was a significant interaction between ZnO NPs and food types on the reproduction of D. magna (Table 1). When food did not contain toxic Microcystis, all the three reproduction parameters significantly decreased with the increasing ZnO NPs concentrations (Fig. 7). Presence of toxic Microcystis reduced the gap among the effects of different ZnO NPs concentrations on the reproduction performance of D. magna. When the toxic Microcystis was at high proportions (i.e. 80%Chþ20%Ma, 70%Chþ30%Ma), D. magna at low levels (0.10, 0.15 mg L1) of ZnO NPs performed better in reproduction than

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four foods types tended to be narrow, and the same phenomena were also observed in another two reproduction parameters. In addition, the number (neonates of first brood per female, total offspring per female, broods per female) decreased to a minimum when the concentration of ZnO NPs was the highest (0.20 mg L1). Above results indicated that low concentration of NPs weaken the negative effects of toxic Microcystis on D. magna reproduction, with the factor of ZnO NPs dominated the effect on D. magna reproductive performance in general trend. 4. Discussion The present study compared different toxic effects of ZnO NPs to D. magna under various food conditions, which was essential for aquatic organisms as they are not only harmed by the pollutants in the ambient environment, but their suffered ecotoxicological effects also depend on food composition (Lyu et al., 2016c; Winner et al., 2006). We found that ZnO NPs and toxic Microcystis had significant negative effects on the key parameters of D. magna life history, and there was an interaction between ZnO NPs and toxic Microcystis, that is, the presence of toxic Microcystis in the food reduced the harmful effect of low concentrations (0.10, 0.15 mg L1) of ZnO NPs to D. magna, indicating that stress caused by ZnO NPs can be disturbed by toxic effects of cyanobacteria, which was consistent with our hypothesis. 4.1. Stability and the total Zn of ZnO NPs test solution The NPs characterization showed a highly dynamic and complex behavior, since the formation of aggregates is mainly dependent on the surface charge density of the particles, ionic strength, pH, and hardness (El Badawy et al., 2010). NPs will aggregate when the surface charge is low, as highly positive or negative charged NPs will repel each other, generating a greater stability (Bagwe et al., 2006). These results indicated that NPs will not remain as single particles when they enter the aquatic environment. The dissolution of NPs is closely related with various elements, including the size of the NPs (Sankar et al., 2014), the exposure concentration and water chemistry (Li and Wang, 2013). In our experiment, the measured total Zn concentrations were only slightly lower than nominal levels, which meant that the test organisms were exposed in relatively real settings of different concentrations. During the exposure, the stock NPs solution was prepared in the early stage every other day to keep a relatively stable state. Nevertheless, there still exists many controversies on the action form of NPs cytotoxity about the contribution of NPs itself and the ions it dissolves to the overall toxicity (Adam et al., 2014; Santo et al., 2014; Xiao et al., 2015). Moreover, some studies that used the corresponding Zn salt as comparable experiments concluded that the toxicity was similar to that of dissolved ions (Bacchetta et al., 2016, 2017). Hence, the total Zn (NPs itself and the dissolved ions) content in our study was ready to maximize the toxicity effect on behalf of the overall ZnO NPs. Fig. 2. Changes in Zn concentrations under different treatments. Some error bars are too short and covered by the date symbol. The black and white dots represent initial and 24-h actual Zn concentration in the testing medium, respectively.

those in the treatments without ZnO NPs, then the number of these three reproduction parameters decreased slowly with the increase of ZnO NPs concentration. When the ZnO NPs concentration was 0.15 mg L1, the gap of the quantities of total offspring under the

4.2. Toxicity of ZnO NPs on D. magna under different food types After the exposure of 21 days, the mortality occurred (Fig. 5) and reproduction significantly reduced (Fig. 7) in ZnO NPs and Microcystis treatments, which indicated that the concentration of ZnO NPs and Microcystis caused chronic toxicity on D. magna. Both ZnO NPs and Microcystis delayed the development of D. magna, but there was no interaction between ZnO NPs and Microcystis on the time at maturation and first brood except for body length at

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maturation of D. magna. Previous studies showed that significant decline in body growth at maturation of Daphnia was detected with the presence of NPs concentration (Zhao et al., 2012) and toxic Microcystis (Lyu et al., 2019). Nonetheless, in our experiment, when the Daphnia was fed low quality food of toxic Microcystis and exposed to ZnO NPs simultaneously, the decline trend became relaxed with the increase of the ZnO NPs concentration, indicating that ZnO NPs may buffer the detrimental effects of toxic Microcystis on Daphnia commutatively in a certain range of concentrations. As the concentration of ZnO NPs increased, mortality rate rose and growth and reproduction decreased under completely good food of 100%Ch (Fig. 5a), which can be explained by previous study that ZnO NPs affect the genes related to reproduction, transport of cytoskeletal, and cellular respiration in Daphnia (Poynton et al., 2011). Furthermore, they can inhibit the expression of genes involved in reproduction, for instance, genes related to eggshell proteins, resulting in serious health and fertility problems (Poynton et al., 2011). Since metabolism, detoxification, and repair require extra energy, under such chemical stress, Daphnia may allocate energy from the reproductive process to its defense (Vandenbrouck et al., 2011). Many species of cyanobacteria produce toxins that may cause the death of Daphnia (Lyu et al., 2014, 2015). In agreement with these results, when D. magna not exposed to ZnO NPs, mortality was increased with the increasing proportion of toxic Microcystis in the food (Fig. 5). For the parameters of reproduction (neonates of first brood, total offspring per female, number of broods per female) of D. magna, low concentration of ZnO NPs (0.10, 0.15 mg L1) can improve the offspring and broods per female when compared to the treatments without ZnO NPs under the mixed food of toxic Microcystis (Fig. 7). The mortality rates of ZnO NPs at 0.10 and 0.15 mg L1 were all lower than those in the treatments without ZnO NPs under the mixed food of high proportion toxic Microcystis (Fig. 5c and d). These results added substantial evidence to prove our speculation that certain concentration ranges of ZnO NPs and toxic Microcystis can mutually weaken their harmful effects on D. magna. Moreover, the total Zn content in D. magna increased with the increasing concentrations of the ZnO NPs Daphnia were exposed (Fig. 3d), suggesting that Daphnia adsorbed and accumulated Zn to the carapace and/or internalization of body. Our data showed that uptake of ZnO NPs in Daphnia was also dependent on food composition in the test solution. From this point of view, it was possible that other mechanisms may be related to this and are not just due to the accumulation of zinc in the body because the degrees of toxic effects from diet and filtering seemed different. ZnO NPs may cause damage to the mitochondria since a large amount of zinc may enter cells, and as a result, reducing the reproduction and growth of Daphnia (Bacchetta et al., 2017). Moreover, the NPs attached to the carapace are negligible due to only 10e16% of the Zn in the NPs adhere to the outside of the carapace (Li and Wang, 2013). Previous studies found that Daphnia food intake decreased in the presence of NPs, and oxidative stress was also induced (Dominguez et al., 2015). Here in the present study, at low concentrations of NPs, probably the reduction of food intake including toxic Microcystis reduced the mortality rate. The physical effects of false food satiety may result in reduced food intake in the presence of NPs, and thus caused less energy available due to less food uptake. These results suggested that dietary metals specifically targeted for reproduction and energy storage.

Fig. 3. Total Zn in algae (12 and 24 h) and D. magna (21 d) following 0.10, 0.15 and 0.20 mg L1 exposure concentrations through different food exposure scenarios

(DW ¼ Dry Weight). The error bar represents the standard error of sample replicates. Some error bars are too short and covered by the date symbol.

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Fig. 4. SEM images of mixed algae (80%Chþ20%Ma) exposed to no NPs (A1eA3), 0.10 mg L1 (B1eB3), and 0.15 mg L1 (C1eC3) ZnO NPs for 2 days.

4.3. The potential environmental implications of combined effects of Microcystis and ZnO NPs on D. magna As for the attenuation effect of ZnO NPs on Daphnia with the existence of toxic Microcystis, our speculation was that ZnO NPs can reduce the toxicity of Microcystis. Some studies have reported NPs inhibit the growth of M. aeruginosa (Sankar et al., 2014). Metal oxide NPs have antibacterial and antifungal effects and can effectively inhibit the growth of various microorganisms (Raffi et al., 2010). Furthermore, NPs attached to the surface of the algae were observed under the SEM (Fig. 4), though internalization of NPs has not been directly confirmed in this study. The NPs can form aggregates in the medium that capture and encapsulate the algae cells, which can probably contribute to algal growth inhibition (Ji et al., 2011). It should be noted that ZnO NPs can release Zn2þ which could be combined with the surface of algae or be internalized by algal cells (Chen et al., 2017), and thus have the potential to be transferred to D. magna during the feeding period. Additionally, Zn can transfer through the food chain and has the ability of internal regulation of Zn (Muyssen and Janssen, 2002). Note the characteristic of D. magna, as no-selective filter feeders, they can ingest particles smaller than the size of 70 mm (Geller and Muller,

1981). Therefore, the ZnO NPs in our study can be taken up by Daphnia via filtering directly, besides through ingesting food. Previous studies have suggested that NPs combining food sources can affect animals' health at higher trophic levels (Croteau et al., 2014; McTeer et al., 2014). For example, Chen and colleagues reported TiO2 NPs could be accumulated in Daphnia from algae in the food chain (Chen et al., 2015). When Daphnia exposed to NPs were feed to zebrafish, which could cause an adverse impact on the digestive enzyme activities of zebrafish (Fouqueray et al., 2013). Recent studies have also demonstrated that ZnO particles can be transferred from algae to Daphnia through the dietary route (Chen et al., 2017; Bhuvaneshwari et al., 2018). However, good quality food (Scenedesmus obliquus or Chlorella) was fed to Daphnia in these studies (Chen et al., 2017; Bhuvaneshwari et al., 2018), which were different from our food composition combining with different proportions of toxic Microcystis. Some studies suggested ZnO NPs are toxic to multiple generations of algae (Franklin et al., 2007; Aruoja et al., 2009). Manzo et al. (2013) also showed the photosynthetic system of algae is influenced by the ZnO NPs which can result in shading effects and mechanical injury (Manzo et al., 2013). The CuO NPs significantly inhibit the growth and photosynthetic pigment contents of toxic

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Fig. 5. Mortality rate of Daphnia in different treatments. Uppercase (A, B, C) characters indicate significant differences in mortality rate among different NPs concentrations under various food types, respectively.

Table 1 Two-way ANOVA on reproduction and growth of Daphnia subjected to various ZnO NPs levels and food types. Life-history parameters Time to maturation Food types (A) NPs concentration (B) AxB Time to first brood Food types (A) NPs concentration (B) AxB Body length at maturation Food types (A) NPs concentration (B) AxB Neonates of 1st brood per female Food types (A) NPs concentration (B) AxB Total offspring per female Food types (A) NPs concentration (B) AxB Number of broods per female Food types (A) NPs concentration (B) AxB

DF

SS

MS

F

3 2 6

102.331 216.58 15.928

34.11 108.29 2.655

18.076 <0.001 57.386 <0.001 1.407 0.223

3 2 6

106.446 196.583 5.571

35.482 98.291 0.928

23.041 <0.001 63.829 <0.001 0.603 0.727

3 2 6

1.099 0.0614 0.764

0.366 0.0307 0.127

29.697 <0.001 2.487 0.09 10.32 <0.001

3 3 9

398.625 875.625 472.725

132.875 291.875 52.525

15.709 <0.001 34.507 <0.001 6.21 <0.001

3 3 9

18793.15 6264.383 16215.5 5405.167 17928.75 1992.083

55.078 <0.001 47.523 <0.001 17.515 <0.001

3 3 9

46.203 108.922 48.146

31.272 <0.001 73.723 <0.001 10.862 <0.001

15.401 36.307 5.35

P

M. aeruginosa, exhibiting the cytotoxicity through enhancing ROS generation against M. aeruginosa and the loss of membrane integrity (Sankar et al., 2014). Only a few studies reported that ZnO NPs cause the shading and mechanical damage on M. aeruginosa,

destroying organelles, and result in the inhibition of algal growth ultimately (Xue et al., 2014). We should also note that NPs not only inhibit toxic Microcystis but also Chlorella (Ji et al., 2011; Sadiq et al., 2011; Oukarroum et al., 2012), but we cannot distinguish which cells were damaged more seriously and which algae adhered more ZnO NPs under SEM electron microscopy. As ZnO NPs can also cause toxicological effects on different green algae, such as Chlorococcum sp., Scenedesmus rubescens, and Chlorella vulgaris (Aravantinou et al., 2015; Pendashte et al., 2013), which may reduce the availability of good food for Daphnia, therefore, neutralization of toxicity between toxic Microcystis and ZnO NPs on D. magna needs to be carefully considered in natural waters. 5. Conclusions Our findings demonstrated that both toxic Microcystis and ZnO NPs significantly delayed the development of D. magna to maturation and reduced the reproductive performance of D. magna. Presence of toxic Microcystis reduced the gap among the effects of different ZnO NPs concentrations on the reproductive performance of D. magna. When the toxic Microcystis in the food composition was at high proportions (i.e. 20% and 30%), D. magna at low levels (0.10 and 0.15 mg L1) of NPs performed better in reproduction than those in the treatments without ZnO NPs. When ZnO NPs concentration was at 0.15 mg L1, the gap of the reproductive performance among different proportions of toxic Microcystis in the food tended to be narrow. With the proportion of toxic Microcystis increased, the mortality rate of maternal D. magna exposed to ZnO NPs at 0.10 and 0.15 mg L1 were all significantly lower than the treatment without ZnO NPs. In conclusion, low concentration of

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Fig. 6. The effect on a range of parameters measured on the first brood: the time to maturation (a); the time to first brood (b); the body length at maturation (c); dots are mean measurements, and error bars are standard error.

Fig. 7. Reproductive performances of Daphnia in different treatments: neonates at first brood (a); total offspring per female over this lifespan (b); the number of broods the mother produced over this time (c). Dots are mean measurements, and error bars are standard error.

Conflicts of interest ZnO NPs and toxic Microcystis can mutually attenuate their harmful effects on D. magna, which has significantly implications in appropriately assessing the ecotoxicological effects of emerging pollutants in a complex food conditions in the field.

The authors declare no actual or potential conflict of interest. Acknowledgements We greatly appreciate the two anonymous reviewers for their

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constructive comments. This study was supported by the National Natural Science Foundation of China (31730105), “333 High Level Talent Project” in Jiangsu Province (BRA2017452), Young Elite Scientists Sponsorship Program by CAST and ISZS (ISZS-YESS Program), and the Priority Academic Program Development of Jiangsu Higher Education Institutions. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.chemosphere.2019.05.269. References Adam, N., Schmitt, C., Galceran, J., Companys, E., Vakurov, A., Wallace, R., Knapen, D., Blust, R., 2014. The chronic toxicity of ZnO nanoparticles and ZnCl2 to Daphnia magna and the use of different methods to assess nanoparticle aggregation and dissolution. Nanotoxicology 8, 709e717. Aravantinou, A.F., Tsarpali, V., Dailianis, S., Manariotis, I.D., 2015. Effect of cultivation media on the toxicity of ZnO nanoparticles to freshwater and marine microalgae. Ecotoxicol. Environ. Saf. 114, 109e116. 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