metalloids in willow catkins collected in urban parks of Beijing and their health risks to human beings

Science of the Total Environment 717 (2020) 137240

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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

Bioaccessibility of metals/metalloids in willow catkins collected in urban parks of Beijing and their health risks to human beings Xiaoming Wan a,b,⁎, Gaoquan Gu a,b, Mei Lei a,b, Weibin Zeng a,b a b

Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China University of Chinese Academy of Sciences, Beijing 100089, China

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

• Fine particles (b10 μm) are attached to the surface of catkins. • Bioaccessibility of metals/metalloids in catkins was higher than that in dusts. • Correlation was found between Pb in catkin and Pb in dust. • Potential risks of catkins need to consider in contaminated areas.

a r t i c l e

i n f o

Article history: Received 13 January 2020 Received in revised form 2 February 2020 Accepted 8 February 2020 Available online 10 February 2020 Editor: Daqiang Yin Keywords: Lung bioaccessibility Catkin Dust Fine particle Metal/metalloid

a b s t r a c t Air pollution and its resulting health risks in Beijing City have been widely investigated by scientists and administrators. However, the health risks caused by willow and poplar catkins in April and May (known as “spring snow”) have been rarely reported. Poplar and willow are the two common trees in Beijing City that generate many whirling catkins in the air. The chemical composition of catkins remains unknown. In this study, catkins and dust samples were collected in several parks in Beijing. The total concentrations of metals/metalloids in catkins measured through inductively coupled plasma mass spectrometry were generally lower than those of the corresponding dust samples, and they were lower than the risk control standard for soil contamination of development land. The simulated rain and lung fluid extraction rates of catkin samples were significantly higher than those of the dust samples. The concentration of extracted Pb and Zn using simulated rainwater exceeded the environmental quality standards for surface water (0.1 and 2.0 mg/L for Pb and Zn, respectively), indicating the possibility of runoff pollution. Scanning electron microscopy images showed that fine particles (b10 μm) are attached to the surface of catkins. Therefore, the metals/metalloids in fine particles adsorbed by the catkin samples possess higher bioaccessibility than that in the dust samples based on different sizes of particles. A significant correlation is found between Pb in catkin and Pb in dust. Therefore, attention should be paid to the possible increase in metal/metalloid concentrations in catkins planted in contaminated areas. © 2020 Elsevier B.V. All rights reserved.

⁎ Corresponding author at: Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China. E-mail address: [email protected] (X. Wan).

https://doi.org/10.1016/j.scitotenv.2020.137240 0048-9697/© 2020 Elsevier B.V. All rights reserved.

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1. Introduction Air pollution is a major environmental risk to human health (Han et al., 2017). Outdoor air pollution and particulate matter from outdoor air pollution have been classified as carcinogenic to humans (IARC Group 1), based on enough evidence of carcinogenicity in humans and experimental animals (Loomis et al., 2013). Negative effects of air pollution on cardiovascular and respiratory health have been indicated (Liu et al., 2018; Tang et al., 2018). The World Health Organization (WHO) indicates that air pollution is responsible for approximately 7 million premature deaths per year caused by the increased mortality from stroke, heart disease, chronic obstructive pulmonary disease, lung cancer, and acute respiratory infections (WHO, 2019). Outdoor air pollution contributes to four out of seven of these deaths, whereas indoor smoke is responsible for the rest. Such health risks caused by air pollution are particularly serious in developing countries because of rapid urbanization and fast population growth (Luo et al., 2019; Zhu et al., 2019). Air pollution ranks as one of the top causes of death in China, accounting for a mortality of approximately one order of magnitude higher than that caused by road transport injuries and Human Immunodeficiency Virus/Acquired Immune Deficiency Syndrome (Lelieveld et al., 2015). Air pollutants can be classified as gaseous pollutants (such as carbon monoxide, sulfur dioxide, nitrogen oxides, volatile organic compounds, and ozone), persistent organic pollutants, inorganic trace elements, and respirable particulate matter (PM2.5 and PM10). At present, PM2.5 is a serious contaminant that can easily enter and damage human bodies, leading to various respiratory and cardiopulmonary diseases (Domínguez-Vilches et al., 1995; Al-Hemoud et al., 2019). Long-term exposure to respirable PM at 100 μg m−3 could shorten the average life expectancy by three years (Chen et al., 2013). Although Beijing, the capital city of China, has achieved huge improvement in air quality, its PM2.5 concentration (25 μg m−3) for 138 days in 2018 is still above the recommended air quality standard by the WHO (WHO, 2006; BMEPB, 2019). Spring and winter are the seasons with severe PM2.5 contamination in Beijing (Shi et al., 2019). The high concentrations of PM2.5 and PM10 in spring might be contributed by the whirling catkins (flowers) of planetree (Platanus), willow (Salix) and poplar (Populus) to some extent (Zhou et al., 2019). Willows and poplars have been widely planted in China to produce wood and to combat desertification because they are easy to plant and grow fast. A report in 2003 indicated that poplar accounts for 13.5% of the total forest plantation area in China (Society and Commission, 2003; Luo et al., 2019). The planted poplar area was about 4,900,000 ha, accounting for 73% of the world's total poplar plantation area (Ball et al., 2005). The planted poplar and willow in China accounts for 85% of worldwide poplar and willow resources in planted forests and agroforestry systems (FAO, 2008). In Beijing area, 84 million female poplar or willow trees that can produce catkins are planted in Beijing area during the 1960s and 70s (Ma, 2014). According to the latest statistics given by Beijing Gardening and Greening Bureau in 2018, there are still 284,000 female poplar and willow trees that can produce catkins in the urban areas of Beijing (Wang, 2019). In the flowering season (usually April and May), whirling willow and poplar catkins can be found in the outdoors or parks and are widely present in offices, shopping malls, and households. Each poplar tree can produce 25 kg catkins (Wu et al., 2019), implying that 7.1 million kg catkins can be produced in the urban areas of Beijing, thereby immensely contributing to the emissions of particles in spring. Such a large number of plant-related particles can account for approximately 2%–10% of the total number of particles (Zhou et al., 2019). Because of the whirling catkins in late spring and early summer, residents may experience coughing, eye irritation, and other allergic symptoms (Li et al., 2016b; Wu et al., 2019). Compared with other particle-shaped pollens, catkins have large surface area to adsorb large amounts of fine particles (Wei et al., 2019). Therefore, they also have the potentials to absorb pollutant

particles. Catkins have been pyrolyzed into biochar because of their large area and capacity to adsorb pollutants, showing high removal of organic and inorganic pollutants (Zalesny et al., 2009). During the whirling–landing–whirling cycle of catkins, their fruit hairs may rupture because of mechanical force, thereby producing inhalable PM2.5 and PM10 and posing health risks to human beings (Zhou et al., 2019). Few studies have been conducted on the chemical compositions and potential health risks of catkins. Does whirling catkins adsorb pollutants as fine particles? What types of pollutants exist in fine particles, and what is the lung bioaccessibility of these particles? This study collected catkin samples and corresponding dust samples in several parks of Beijing City to answer these questions. The metal/metalloid concentrations in catkins were investigated. The total concentrations, simulated rainwater extracted fractions, and simulated lung fluid extracted fractions of metals/metalloids in catkins were measured and compared with those of the corresponding dust samples. The morphological characteristics of catkins were analyzed through scanning electron microscopy (SEM). 2. Materials and methods 2.1. Sampling Sampling was conducted in 13 parks where catkins are visible in the sky and on the ground during the flowering season of willow and poplar from April 10 to May 15, 2019. The sampling locations are distributed in five districts of Beijing, China (Fig. 1). The five districts are Yanqing, Haidian, Chaoyang, Xicheng, and Fengtai, from north to south. Yanqing is a suburban district in the northern mountainous part and is dedicated to ecological conservation. Xicheng is a traditional inner-city district and currently the capital functional core area. Chaoyang, Haidian, and Fengtai are urban functional expansion areas, with Fengtai as the southmost district in this study. Three sampling sites were selected randomly in each park. At every sampling site, the catkins were trapped at the height of ~1.5 m using a pump-connected filter with an aperture diameter of 10 μm. In order to get enough samples for the chemical analysis, the sampling duration varied at different sites depending on the density of catkins in the air. Filters were weighed before and after dust collection using a microbalance (C-35; Cahn, Paramount, CA) with a sensitivity of 1 μg to calculate the weight of catkins. The density of catkins can be calculated based on their weight and the air volume recorded by the pump for subsequent risk assessment. Dust samples were collected using disposable brushes and polyethylene zipper bags at the same sites where catkins are collected. At each sampling site, three subsamples of dust were collected from sidewalks or pedestrian roads in urban parks, and then mixed together as one composite dust sample. The dust samples were sieved through a 100 μm screen. Catkins visible to the naked eye in the dust samples were manually removed. 2.2. Analysis of the total concentration of metals/metalloids in catkins and dust Catkin and dust samples were dried in separate desiccators at room temperature for 24 h. Microwave digestion was used to determine the total concentrations. General digestion followed the 3050B method of the USEPA (USEPA, 1996). Samples (0.5 g) were carefully weighed and placed in digestion tubes. Nitric acid (5 mL) was added to each tube, and 3 mL hydrogen peroxide was added to each tube after 24 h. Then, microwave digestion started for 6 min at 120 °C, followed by 6 min at 150 °C, and 6 min at 180 °C. The solution volume (25 mL) was filtered using a 0.45 μm filter. The resulting digestate was diluted at 1:10 ratio with 1% HNO3 to analyze the metal/metalloid concentrations through inductively coupled plasma mass spectrometry (ICP– MS). Calibration curve accuracy was confirmed based on a certified reference material (SRM 1640a, Natural Water from National Institute of

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Fig. 1. Sampling locations for catkin and dust samples in Beijing City.

Standards and Technology). ERM CC141 loam soil was digested with the collected samples for quality control and recovery assurance. The levels of the analyzed elements in the reference material were consistent and within the ranges of the certified values. The recovery rates of As, Cd, Cu, Ni, Pb, and Zn were 91%–105%, 82%–101%, 95%–102%, 95%–110%, 98%– 101%, and 96%–108%, respectively. 2.3. Simulated rainwater and simulated lung fluid extraction of metals/metalloids from catkins and dust An appropriate amount of diluted nitric acid was added to Milli-Q water (18 MΩ·cm, Milli-Q water purification system, Millipore Corporation) to simulate rainwater, reaching a pH of 5.0, which is the recommended pH for simulating rainwater in the United States (USEPA, 1986). The simulated lung fluid was the same as that described by (Gray et al., 2010). It contained 6800 mg NaCl L−1, 5300 mg NH4Cl L−1, 2300 mg NaHCO3 L−1, 1200 mg H3PO4 L−1, 1700 mg NaH2PO4·H20 L−1, 630 mg Na2CO3 L−1, 580 mg Na acetate L−1, 200 mg K acid phthalate L−1, 450 glycine mg/L, 510 mg H2SO4 L−1, 590 mg Na3 citrate·2H2O L−1, 290 mg CaCl2·2H2O L−1, and 420 mg citric acid·H2O L−1 and was adjusted to pH 7.4 using HCl. The ratio of 1:20 (w/v) was used in the extraction of simulated rainwater and lung fluid. The extraction followed the procedure described by Gray et al. (2010). The catkin or dust samples were rotated (33 rpm) in an incubator for 24 h at a constant temperature (37 °C). This period is considered adequate to achieve equilibrium in the metal dissolution of the simulated fluid. Then, the samples were centrifuged for 15 min at 2500 rpm. The supernatant was filtered through a 0.45 μm filter. The filtrates were stored in the refrigerator and maintained at 4 °C until ICPMS analysis. Each sample had three replicates. 2.4. Energy-dispersive X-ray spectroscopy (EDS)–SEM analysis The microscopic features of catkins were characterized using a scanning electron micro-scope (FEI Scios DualBeam FIB/SEM, USA) equipped with an Oxford X-Max Energy Dispersive X-ray Spectroscopy (EDS) Detector. The detailed procedure has been described in Li et al. (2005). 2.5. Risk assessment Carcinogenic risks were not calculated because the exposure to contaminants in catkins is short-term and not all the metals/metalloids considered in this study have a known slope factor. For the

noncarcinogenic risks, inhalation was considered the main exposure pathway of metals/metalloids in catkins to human beings. Therefore, only the health risks through inhalation were calculated, which can be expressed as Eqs. (1) and (2) (Li et al., 2019):

ADDinh ¼

C  InhR  EF  ED PEF  BW  AT

HQ ¼ ADDinh =RfD;

ð1Þ

ð2Þ

where ADDinh is the dose of metals/metalloids received through inhalation of particles (mg kg −1 day−1), C is the concentration of metals/metalloids in catkins or dust (mg kg−1), InhR is the inhalation rate (default value is 20 m3/day), EF is the exposure frequency (60 day year−1), ED is the exposure duration (not specified because ED exists in the numerator and denominator), PEF is the particle emission factor (use the value obtained from the catkin collector, m3 kg−1), BW is the body weight (default value, 70 kg), AT is the average time (default value: 365 × ED), HQ is the hazardous quotient indicating the risk level of human exposure, and RfD is the reference values of metals/metalloids received through inhalation of particles (mg kg −1 day−1). The RfD values for As, Cd, Cu, Ni, Pb, and Zn were 4.29 × 10−6, 1.00 × 10−3, 4.02 × 10−2, − 2.06 × 10−2, 3.52 × 10−3, and 3.00 × 10−1 mg kg−1 BW day 1, respectively (Li et al., 2019). The overall noncarcinogenic risk posed by all the considered metals/ metalloids (indicated as HI) was calculated as the sum of the HQ values of individual metals, which can be expressed as Eq. (3): 6

HI ¼ ∑i¼1 HQi

ð3Þ

2.6. Statistical analysis SPSS 19.0 (IBM, USA) was used to conduct the correlation analysis among the different metals/metalloids in catkins (Peng et al., 2019), and the pairwise correlation of a certain element between the catkin and the corresponding dust sample was obtained. Origin 9.0 was used to construct the graphs. The significance level was set to an error probability of 0.05.

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Fig. 2. SEM image (a) and chemical composition of catkin (b) and the particles attached to the catkin surface (c).

Fig. 3. Total concentrations and extracted concentrations of arsenic (a), cadmium (b), copper (c), nickel (d), lead (e), and zinc (f) in the catkins. The lower and upper hinges correspond to the 25th and 75th percentiles, the horizontal line to the median, and the whiskers to 1.5 × the IQR (approx. 95% percentile). The square shows the mean.

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3. Results and discussion 3.1. Chemical compositions of catkins The SEM image clearly indicated that some dust particles with size b10 μm are attached to the catkin surface (Fig. 2a). The EDS results indicated the different chemical compositions of catkins and the particles attached to the catkins. The chemical composition of catkins was similar to biomass, with a large percentage of carbon (Fig. 2b). The chemical composition of the adsorbed particles was similar to the soil (Fig. 2c), with high concentrations of Si and small amounts of trace elements (Zhang et al., 2019). Catkins float in the air, occasionally deposit on the ground, and float again with the wind. During this resuspension process, dust might be adsorbed by the catkins. Only fine particles with low weight can travel

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together with the catkins because of gravity, and these fine particles are more enriched with contaminants compared to particles with larger sizes (Zhang et al., 2013; Lanzerstorfer, 2018; Nie et al., 2018). With an increase in the dust size from 2 μm to 500 μm, the metal concentrations in dust decrease (Logiewa et al., 2019). Because of their special fiber characteristics, some studies have been conducted on the potential recycling methods of catkins (Wang et al., 2017; Shi et al., 2019). However, caution should be taken when using this material because of its large tendency to adsorb fine dust particles. 3.2. Total concentrations of extracted metals/metalloids in catkins and dust The total concentrations of metals/metalloids in catkins were in the order of As/Cd b Cu/Ni/Pb b Zn (Fig. 3). The concentrations of extracted metals/metalloids in simulated rainwater followed the same order as

Fig. 4. Total concentrations and extracted concentrations of arsenic (a), cadmium (b), copper (c), nickel (d), lead (e), and zinc (f) in the dust. The lower and upper hinges correspond to the 25th and 75th percentiles, the horizontal line to the median, and the whiskers to 1.5 × the IQR (approx. 95% percentile). The square shows the mean.

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the total concentrations. The concentrations of Pb and Zn in the runoff test were higher than the environmental quality standards for surface water (2.0 and 0.1 mg/L for Zn and Pb, respectively) established by the Ministry of Ecology and Environment of the People's Republic of China (MEEP, 2002), thereby indicating the risk of contaminants in catkins transferring to water. The concentrations of extracted metals/metalloids in simulated lung fluid were slightly higher than that extracted in simulated rainwater. This might be related to the PO3− 4 , acetate, glycine, citrate and citric acid used in the simulated lung fluid, which can act as the competing ions or chelating ligands for these trace elements, thus increasing the extraction rate (Isosaari and Sillanpää, 2012; Ehsan et al., 2014). The total concentrations of metals/metalloids in dust were higher than that in catkins and followed the order of Cd b As/Ni b Cu/Pb b Zn (Fig. 4). Like the catkin results, the extractable fractions of all the six metals/metalloids only accounted for a small percentage of the total concentrations. Compared with the total concentrations of metals/metalloids in the particulate (Liu et al., 2019) and dust samples elsewhere (Cheng et al., 2018), the concentrations of metals/metalloids were generally within the same range, with lower concentrations of As and Pb in the dust samples in the current study. This finding is because sampling is mainly conducted in parks, where pollution from traffic or industry is limited. The correlation analysis (data provided in the supplementary material Table S1, S2 and S3) among the different elements in catkin samples found significant correlations between As and Cd, As and Pb, Cd and Pb, Cu and Pb, Ni and Pb (P b 0.05). In the dust samples, only As and Cd showed significant correlation (P b 0.05). The correlation of metal/metalloid concentrations between the catkin and the corresponding dust samples found that the concentration of Pb in catkins was significantly correlated with Pb in dust (P b 0.05), whereas no significant correlation was found for other metals/metalloids (P N 0.05). Poplar and willow have been widely used to extract, immobilize, and degrade pollutants in the soil because of their fast growth and tolerance to pollutants (Vervaeke et al., 2003; Zalesny et al., 2009). Considering the correlation between contaminants in catkins and dust, the potential

risks of excess pollutants in catkins to human beings in contaminated areas must be considered. Furthermore, the Ni, Zn, Pb, Cd, and Cu concentrations increase by fourfold in the vegetative tissues of poplar in urban areas compared with those in clean areas (Sluchyk et al., 2014). Similarly, the concentrations of Zn and Cd in catkins from contaminated areas are significantly higher than that from noncontaminated areas (Madejón et al., 2013). Therefore, the potential increase in pollutant concentrations of catkins might be caused by the increased concentration of pollutants in the dust and plant tissues. The concentration of Cd in several dust samples exceeded the screening value (4.0 mg kg−1, pH N 7.5) regulated by the soil environmental quality risk control standard for soil contamination of agricultural land (MEEP, 2018). Beijing residents typically plant vegetables in their balconies. However, urban dust might lead to the accumulation of Cd in the balcony crops through uptake from soil or direct atmospheric deposition. The extraction rates of metals/metalloids varied among different environmental media, extraction methods, and metals/metalloids. The metals/metalloids with the lowest simulated rainwater extraction rates for dust and catkin samples were As and Pb (Fig. 5). It is known that Pb has low bioavailability in soil or dust (Zhong et al., 2020). The low extraction rate of As may be related to the extraction method, which might work better in ions rather than anions. The existence form of As in the dust might be another reason, determining the low bioaccessibility of As on the basis of previous studies (Huang et al., 2014). Cd showed higher extraction rates than those of the other five elements (Fig. 5), thereby implying its comparatively high bioaccessibility, which is consistent with the results of previous studies on the bioaccessibility of Cd in soils and PM (Li et al., 2016a; Liu et al., 2019). The extraction rates of metals/metalloids from catkins showed approximately the same trend with that of dust but with higher rate. For example, the Cd extraction rate of simulated rainwater from dust was lower than 10%, whereas that from catkins reached up to 22%. This trend was observed for all the metals/metalloids and the simulated extractions of water and lung fluid.

Fig. 5. Water extraction rates (a & b) and simulated lung fluid extraction rates (c & d) of metals/metalloids from catkin and dust. The lower and upper hinges correspond to the 25th and 75th percentiles, the horizontal line to the median, and the whiskers to 1.5 × the IQR (approx. 95% percentile). The square shows the mean.

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The higher extraction rates from catkin than dust could be explained by two reasons, namely, (1) the total concentration of metals/metalloids in catkins was lower, leading to a higher mathematical uncertainty and (2) the bioaccessibility of metals/metalloids in catkins was higher. The particles that can be adsorbed and carried by catkins have small sizes. As shown in the SEM image, the size of adsorbed particles was smaller than 10 μm (Fig. 2a). Metals/metalloids in the soil tend to be adsorbed to small particles. Studies have shown that fine fractions of dust have high metal concentrations and high bioaccessibility when an anthropogenic origin is found (Acosta et al., 2011; Goix et al., 2016). Compared with the bulk sample (b2000 μm), the bioaccessible concentrations of As, Cd, and Pb in the dust particles with a size of 2–20 μm were higher by 73%, 65%, and 55%, respectively (Goix et al., 2016). Similarly, higher bioaccessible As concentrations were observed in the samples sieved to b45 μm particle size compared with those with larger particle sizes (Meunier et al., 2011). Therefore, the high bioaccessible concentrations of metals/metalloids in catkins may be cause by the

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high bioaccessibility of metals/metalloids in fine particles adsorbed by the catkin samples. Bioaccessibility reflects the fractions of a contaminant available for the biological activities, often used to help predict bioavailability (Ettler et al., 2012). Whereas bioavailability reflects the fractions of a contaminant that are involved in the dissolution, transport and absorption by a receptor organism (Ng et al., 2015). Compared to bioavailability that requires in vivo test, bioaccessibility is comparatively easier to measure. Using total rather than bioaccessible concentrations of particle-bound trace elements has been suggested to overestimate the health risk, and inaccurately identify the high-risk pollution sources (Liu et al., 2019). The bioaccessibility of metals/metalloids has gradually become a more important index than the total concentration. This study revealed that the bioaccessible fractions of metals/metalloids were lower although the total concentrations of metals/metalloids in the dust were apparently higher than those of catkins, thereby implying the potential of catkins to cause health risks to human beings.

Fig. 6. Comparison of total concentrations of metals/metalloids in catkin (a) and dust (b) collected in different districts. The number of sampling sites for catkin/dust was 6, 6, 9, 9, and 9 for Yanqing, Haidian, Chaoyang, Xicheng, and Fengtai district, respectively.

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3.3. Comparison of total concentrations of metals/metalloids in the catkin and dust samples from different districts The total concentrations of As, Cd, Cu, and Pb were generally in the order of Yanqing b Haidian b Chaoyang b Xicheng b Fengtai (Fig. 6), indicating that urban areas had higher concentrations in dust and catkin than that of suburban areas, which is consistent with the literature. Liu et al. (2016) found a clear difference in the metal/metalloid concentrations of dust between rural and urban areas. The average concentration of As in rural dust was 12.4 mg kg−1, which is only half of that in urban dust (24.2 mg kg−1). In the current study, such large difference between urban and suburban areas was observed in As and Pb of dust and catkins, which may come from anthropogenic processes, such as industrial emission, traffic activities, and other processes that may cause the elevated concentrations of metals/metalloids (Lu et al., 2011, Yang et al., 2002). Among the 284,000 catkin-producing poplar and willow trees in the urban areas of Beijing, Chaoyang District showed the highest distribution of female poplar and willow trees, accounting for 37.7% of the total amount (Wang, 2019). Fengtai, Haidian, and Xicheng accounted for 23.2%, 13.0%, and 1.3% of the entire amount of female poplar and willow trees in Beijing City, respectively. As shown in Fig. 6, Chaoyang did not show a significant difference in metal/metalloid concentrations with the other districts. Fengtai, which is the southmost urban district, showed the highest concentrations of Pb, Cu, and Ni, which may be related to the previous industrial production in that area that deposited contaminants in the soil.

3.4. Inhalation risk assessments The health risks caused by catkins or dust in this study were low. The HQ values for As, Cd, Cu, Ni, Pb, and Zn were 0.012, 0.003, 0.004, 0.002, 0.006, and 0.003, respectively. The HI (sum of all the elements) was 0.03. The primary reason for the low risk is that no apparent contamination source is found in these sampling sites. Willow and poplar, especially the former, have been applied to extract or stabilize metals/metalloids in the soil because of their fast growth and tolerance to metal/metalloid pollution (Gordon et al., 1998; Iqbal et al., 2012; Mleczek et al., 2018; Pilipović et al., 2019). The concentrations of metals/metalloids in catkins planted in contaminated areas are expected to be high because of the high concentrations of metals/metalloids in the dust (Blondet et al., 2019). Risk assessments of metals/metalloids in catkins of poplar and willow trees in such areas should be conducted. The largest variance in total concentrations between Yanqing (suburban area) and other districts was found for As and Pb, indicating the high anthropogenic input of the two elements. Cd showed the highest bioaccessibility among the six investigated metals/metalloids. Therefore, the three elements should be the focus of future studies.

4. Conclusions Air pollution and its resulting health risks in Beijing have been widely investigated by scientists and administrators. However, the health risks caused by excessive catkins of willow and poplar in April and May (known as “spring snow”) have been rarely reported. Catkins and dust samples were collected in several districts in Beijing. Although the total concentrations of metals/metalloids in the catkins were lower than that in the dust, the bioaccessibility of these metals/metalloids in catkins was apparently higher than that in the dust. Catkins does not pose unacceptable health risks to human beings through inhalation exposure. However, the possible increase in metal/metalloid concentrations in catkins when planted in contaminated areas as a metal/ metalloid extractor must be considered.

Acknowledgments This work was financially supported by the National Key Research and Development Program of China (Grant no. 2018YFC1800302) and grants from the Youth Innovation Promotion Association of Chinese Academy of Sciences (No. 2017075). 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. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.scitotenv.2020.137240. References Acosta, J.A., Faz, A., Kalbitz, K., Jansen, B., Martinez-Martinez, S., 2011. Heavy metal concentrations in particle size fractions from street dust of Murcia (Spain) as the basis for risk assessment. J. Environ. Monit. 13, 3087–3096. Al-Hemoud, A., Gasana, J., Al-Dabbous, A., Alajeel, A., Al-Shatti, A., Behbehani, W., Malak, M., 2019. 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